Paper - Observations on the peripheral distribution of the nervus terminalis in mammalia (1913)
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Huber GC. and Guild SR. Observations on the peripheral distribution of the nervus terminalis in Mammalia. (1913) Anat. Rec. 7(8): 253-272.
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Observations On The Peripheral Distribution Of The Nervus Terminates In Mammalia
G. Carl Buber And Stacy R. Guild
Laboratory of Histology and Embryology, University of Michigan
Three Figures
Introduction
The occurrence and relations of the nervus terminalis in various types of vertebrates has in recent years been the subject of a relatively large number of contributions, appearing in the main from American laboratories. Johnston in a recent communication summarized this literature in tabular form, and to this the reader is referred for a general consideration. From a study of this literature and from his own contributions, Johnston concludes that, "In all the forms in which the nerve enters the olfactory bulb it as been shown that its fibers pierce the formatio olfactoria to pass on to their proper endings in some part of the forebrain," and further, that the facts appear to show "that the nervus terminalis in most fishes and amphibians is a ganglionated nerve whose root enters the forebrain caudal to the olfactory bulb, usually near the site of the embryonic neuropore, and whose fibers are distributed to the wall of the nasal sac." In this paper Johnston notes the presence, and gives a general description of the nervus terminalis as observed in reptilian and mammalian embiyos, his study including among the latter, pig, sheep and human embryos. His investigation show that in reptilian and mammalian embryos this nerve, "enters the brain at a point somewhat removed from the median plane but otherwise holding the same relation to the primordium hippocampi, precommisural body and neuroporic recess which the root holds in selachians."' The fibers are said to arise from bipolar ganglion cells, collected into a compact ganglion terminale in the pig and human embryos and into several clumps in the course of the nerve and its branches in turtle embryos. So far as concerns the peripheral distribution of the nervus terminalis in mammalia he notes that, "In the pig the nervus terminalis is clearly distributed to the vomeronasal organ," and, "In man the fibers mingle with the olfactory strands of the nasal septum." McCotter has called attention to the presence of a nervus terminalis and a ganglion terminale in adult dogs and cats. These results were obtained in the main by gross dissection, controlled by sections and tissue membranes, spread and stained to admit of study under the microscope. The nervus terminalis was traced to its entrance to the forebrain in both the dog and the cat, ganglion cells were noted in its intracranial course as also small collections of ganglion cells in the septal portion of the vomeronasal nerve just dorsal to the vomeronasal organ. McCotter concludes, "that there is normally present in the adult dog and cat a ganglionated nerve connected with the vomeronasal nerves on the one hand and apparently with the forebrain on the other, having thereby the same morphological relations in these mammals as is described for the nervus terminalis in the lower forms." Johnston's recent studies, above referred to, and as noted in his communication, were made in part on series of embryos in this laboratory.
Our interest in the presence of the nervus terminalis in mammalian embryos having thus been stimulated we were pleased to note a differential staining of this nerve in a series of sagittal sections of the heads of two rabbit embryos, which from size and general development were estimated as having been removed about a week before birth. These heads had been stained after the pyridine-silver method as used by Ranson, with certain modifications to be noted. Our observations on the peripheral distribution of the nervus terminalis in mammalia pertain, therefore, to the rabbit.
Method
The essential steps in the Ranson pyridine-silver technic are as follows: Fixation in ammoniated absolute alcohol; thorough pyridine penetration; thorough washing in distilled water; impregnation with a 2 per cent silver nitrate solution; reduction of the silver by means of a formalin-pyrogallic acid solution. Early in our use of this method we became aware of very evident shrinkage of the nerve cells, probably due to the ammoniated alcohol fixation. This was largely obviated by the injection of the ammoniated alcohol solution into the fresh tissues. The investigations undertaken demanded that the method be made applicable to decalcified tissues. It was found that this could be done by using nitric acid as a decalcifier. The method as now used in this laboratory is as follows : The animal is prepared by chloroform anesthesia and the heart incised before it ceases to beat. This to obtain as complete drainage of the vascular system as is possible. A cannula is then inserted into the main artery supplying the area containing the nervous tissues to be subjected to silver staining and the cannula filled with normal salt solution. By clamping branches the area to be injected can be restricted. A solution consisting of 95 per cent alcohol and a 1 per cent concentrated ammonia is then rapidly injected under a pressure of from 5 to 10 pounds, this being continued until the parts seem well injected. The ganglia, nerve trunks, pieces of the central nervous system, as desired, are then removed and placed in a similar ammoniated alcohol solution, in which they remain for from two to three days. The further treatment is as is given by Ranson for the pyridine-silver method. This method of fixation by a preliminary injection of the ammoniated alcohol solution seems to us to present distinct advantages, especially when used in the study of ganglia and peripheral nerves. For instance, the shrinkage and distortion of the peripheral layers of cells of sensory ganglia is largely obviated. The elements are well fixed and are slightly separated so that much thicker sections may be cut and studied to advantage. The impregnation and reduction of the silver seems more uniform and more certain. The pyridine-silver method as adapted so as to include decalcification of the tissues is as follows: 1. Adult or young animals and embryos of sufficient size to admit of injection are injected with ammoniated alcohol solution, as above described, and the tissues placed in the ammoniated alcohol for from two to four days, depending on the size of the tissue mass to be fixed. 2. Transfer to distilled water, in which the pieces remain until they sink. 3. The pieces are then transferred to a 7 per cent solution of nitric acid, made with distilled water, in which they remain until the decalcification is complete; which varies with the age and size of the tissue block. 4. Wash in distilled water for about one-half hour, the water being changed frequently. 5. The pieces are then transferred to alcohols of 80, 90 and 95 per cent, to each of which is added 1 per cent of concentrated ammonia. A thorough treatment with ammoniated alcohol at this step seems to us essential; three to eight days, depending on the size of the pieces. 6. Rinse in distilled water and place for twenty-four hours in pyridine.
Wash thoroughly in distilled water for twenty-four hours, the water being frequently changed. As the immediate transference of the tissues from the pyridine to the distilled water is liable to result in a swelling of the tissues, which may lead to a bursting of the hemispheres, a gradual transference from the pyridine to the distilled water is recommended. 8. Transfer to a 2 per cent solution of silver nitrate in distilled water, in which the tissues remain for from three to five days, in the dark and at a temperature of about 35°C. 9. Rinse in distilled water and place for from one to two days in a 4 per cent solution of pyrogallic acid in 5 per cent formalin. 10. Dehydrate thoroughly, beginning with 80 per cent alcohol. Aceton may be used to hasten the dehydration, but should be preceded and followed by alcohol. Clear in xylol and embed in paraffin. A necessary stay in the warm oven, even to forty-eight hours, to insure thorough paraffin penetration, does not seem to affect the stain. The possibility of decalcification combined with preliminary ammoniated alcohol injection greatly extends the applicability of the pyridinesilver method. We have found it possible to stain half of the head of a six day rabbit, head and neck of a medium sized frog, head of a small turtle, and so forth. After the injection with the ammoniated alcohol we have removed the skin and exposed the brain.
Further cutting of the pieces was delayed until after the decalcification and second ammoniiated alcohol treatment. The paraffin sections may be cut serially, and fixed to the slide by the water albumen method in the usual way. We are able to confirm Ranson's statement, and find it applicable to the method as here modified, namely, "With fresh pure chemicals, absolutely clean utensils, and a reasonably constant temperature this method can be relied upon to give uniform results."
Material
The material on which our observations on the peripheral distribution of the nervus terminalis in mammalia is based, consists of series of sections of heads of rabbit embryos and young rabbits, cut in the sagittal plane, as follows: a, rabbit embryos, 3 cm. head-breech length; b, rabbit embryos removed about one week before birth: c, young rabbits one day old; d, young rabbit six days old. For the two younger stages the entire head was cut, for the older stages a little over one-half of the head, the series beginning about 2 mm. to the left of the mid sagittal plane, thus including the nasal septum and the entire left half of the brain and head. Two complete sagittal series of each of the three younger stages are at our disposal and one complete sagittal series of the oldest stage. In each of these series the fibers of the nervus terminalis, throughout their entire course, are stained deeply brown or black and are of relatively fine caliber, while the olfactory formation, and the olfactory nerves including the vomeronasal portion, are colored a light brown and are traced as large compact bundles with sheath cells rather than separate fibers. The differential staining is so distinct and characteristic that the two types of fibers can not well be confused.
Graphic reconstruction of the oral part of the forebrain, the olfactory bulb and nerves, the vomeronasal nerves and the nervus terminalis of the right side have been made for the three younger stages. Of the two younger stages by Guild, of the one day stage by the senior author, as well as a partial reconstruction of the six day stage. The resultant figures of the three stages completely reconstructed are so similar that a publication of all seemed unnecessary. The one day stage was chosen for the reason that the parts sketched were less compactly grouped and can thus be followed in the figure with greater ease. The graphic reconstructions were made with the aid of a camera lucida at a magnification of 75 diameters for the one day stage and 85 diameters for the two younger stages. Doubtful points were controlled under higher powers. By the use of orienting points selected in the sections, field after field was adjusted and the pertinent parts traced in pencil. In the final figure only nerve segments clearly joined were sketched in ink. The right side was chosen for the graphic reconstructions by reason of the fact that the final figures were somewhat easier to make in that in tracing the series, beginning with the nasal septum and proceeding lateralwards, the nervus terminalis was superimposed on the olfactory bulb and nerves. The distribution of this nerve on the left side is, it may be anticipated, the same as that on the right side. As concerns the graphic reconstruction reproduced, we desire to state that while the distribution of the nervus terminalis is, as we believe, correctly given, with the magnification used it was not possible to show in detail the size and number of the component nerve fibers of the several branches of the nerve. In order to make the figure intelligible we found it necessary to emphasize the branches of the nervus terminalis and sketch them as solid black lines and thus bring out disproportionately large certain of the finer branches and connections. The distribution of the ganglion cells as given is based on camera lucida projections. In the final drawing the ganglion cells, for the sake of clearness, are sketched disproportionately large. As stated above in all of our series the nervus terminalis was found differentially stained so that under the magnification used it was possible to distinguish between its branches and those of the olfactory and vomeronasal nerves. Our observations on the superficial origin of the nervus terminalis in mammalia are in harmony with those of other authors who have dealt with this subject. In the rabbit the main portion of the nervus terminalis arises from the ventro-mesial surface of the forebrain ; caudal to the olfactory bulb and stalk and oral to the lamina terminalis. Its origin is not by a single compact bundle and from a limited area, but rather by several smaller bundles or roots which pierce the brain substance rather gradually, in smaller subdivisions. In the two younger stages a smaller root was traced to its entrance in the forebrain, at a region more dorsally placed on the medial surface. In the one day stage this root could not be clearly traced to its entrance in the forebrain. The nervus terminalis passes forward along the ventro-mesial aspect of the olfactory bulb, in the form of a loose plexus consisting of three or four strands joined by anastomoses, to a position mesial to the region where the branches of the vomeronasal nerve unite to form a main strand, just above the cribriform area. In this intracranial portion of the nervus terminalis there are found here and there small groups of ganglion cells, either at nodal points of the plexus or as single cells or clusters of two or three ganglion cells along the course of the nerve filaments, and in all of our series there was observed a relatively larger mass of ganglion cells in the region where the nervus terminalis crosses the vomeronasal nerves. This latter mass we regard as the 'ganglion terminale' of authors. The origin, general course and relations to the olfactory bulb and vomeronasal nerves of the nervus terminalis of the rabbit may be seen in figure 1, which figure duplicates in all essentials the figures obtained by graphic reconstruction of this region for the two younger stages studied and for the six day stage. In its passage through the cribriform area the nervus terminalis accompanies in the main the vomeronasal branches, lying on their mesial aspect. If in our sagittal series of heads of embryos and young rabbits the study is begun with the nasal septum and carried from here to the right, it may be seen that the branches of the nervus terminalis are in the deeper portion of the septal mucosa and are first met with on the mesial surfaces of the vomeronasal branches, which pass mesially to the filaments of the olfactory nerves as they radiate to the different parts of the septum, thus in a deeper plane of the septal mucosa.
Fig. 1 Graphic reconstruction of right side of olfactory bulb and stalk, olfactory and vomeronasal nerve, and nervus terminalis, based on a sagittal series of sections of head of a one-day-old rabbit, stained after the pyridine-silver method, and showing differential staining of the nervus terminalis. The nervus terminalis is given throughout its course in jet black; the olfactory and vomeronasal nerves are given in outline; fb, forebrain; ofb, olfactory bulb; vn, vomeronasal nerve; rnt, roots of nervus terminalis; gt, ganglion terminate; snt, septal distribution of nervus terminalis; cp, cribriform plate; vmo, vomeronasal organ, given in outline. X 10.
In all of our series, terminalis branches are associated with each of the three main branches of the vomeronasal nerve and may be traced with them to their termination in the vomeronasal organ. Scattered along the course of the terminalis branches there are found smaller and larger groups of ganglion cells, even in connection with the end branches of the nervus terminalis found in the mucosa of the vomeronasal organ. Here and there there may be observed anastomosis between terminalis branches accompanying the vomeronasal branches with ganglion cells at nodal points. In all of our series certain of the most dorsally placed filaments of the plexus on the mesial surface of the olfactory bulb leave the fibers accompanying the vomeronasal branches as they pass through the cribriform area and course orally toward the upper and anterior part of the nasal septum, to participate in the formation of a plexus found in the deeper portion of the septal mucosa of this region. In the deeper portion of the septal mucosa anterior or oral to the region crossed by the vomeronasal nerves there is found a distinct plexus of terminalis fibers, associated with numerous small groups of ganglion cells, a plexus which reminds one of the enteric plexus, although the groups of ganglion cells are much smaller and the uniting nerve filaments much finer. That this anterior septal plexus is a part of the nervus terminalis distribution is shown on the one hand by the differential staining as found in our series, on the other hand by the fact that the more dorsally placed filaments of the nervus terminalis may be traced into this plexus as well as branches from the terminalis filaments which accompany the vomeronasal nerves. Numerous small groups of ganglion cells are found at the nodal points of this plexus, the number of ganglion cells constituting such a group varying greatly, varying from one cell to perhaps 10 or 15 cells. We have not observed branches of the nervus terminalis nor ganglion cells in the septal mucosa caudal to the region crossed by the vomeronasal nerves. The general peripheral distribution of the nervus terminalis of the rabbit, as also the disposition of the associated ganglia, is so clearly shown in figure 1, that further and fuller description seems to us unnecessary. In our series it is possible to trace the branches of the trigeminal distribution to the nasal septum. In the main the nerve fibers of trigeminal origin appear to us as somewhat coarser, as stained more intensely black, and as presenting other characteristics, less distinct and more difficult to formulate, but evident to one who has studied the series carefully. The trigeminal branches to the nasal septum were confirmed as such in graphic reconstructions of the two younger stages, and in an incomplete reconstruction of the six day stage. It was found inadvisable to attempt to reproduce trigeminal distribution to the nasal septum in figure 1, since added to the structures already shown, the figure presented too complex a network of fibers to admit of following even the main nerve bundles in the reduced reproduction with any degree of certainty. Two rather large branches of the trigeminal nerve enter this region; a, the rami mediates of the n. nasociliaris and b, the n. nasopalatine. The former is from the first division of the trigeminal nerve and was traced from the Gasserian ganglion into the orbit, where it passes over the optic nerve and forward to enter the cranial cavity through the anterior ethmoidal foramen. Here it passes laterally about the base of the olfactory bulb and enters the nasal cavity through the anterior part of the cribriform plate. The larger rami mediales course along the anterior nasal wall to reach the septum about one third of the way down. Branches from these are distributed over the rostral and anterior part of the septum. The n. nasopalatine was traced from the sphenopalatine ganglion, and at least a part of its fibers appear to have origin in the Gasserian ganglion, passing through the sphenopalatine ganglion. This nerve courses along the posterior part of the nasal septum as it leaves the sphenopalatine ganlion, toward the caudal end of the vomeronasal organ where it divides in two branches; one going to the palate, the other passing along the ventro-lateral border of the vomeronasal organ, giving off numerous branches which course upward and forward to reach the ventral and posterior or caudal portion of the nasal septum. Branches of this nerve are also distributed to the nasal septum caudal to the path of the vomeronasal nerve. Some of the smaller branches of the trigeminal nerve, especially those coming from the nasopalatine branch appear to join the plexus formed on the nasal septum by the nervus terminalis, others remain separate to their terminal twigs. This anastomosis of nerve filaments of Terminalis and Trigeminal origin renders it more to determine the ultimate distribution of each. However, in no case was a ganglion cell or groups of such found on a nerve trunk clearly composed entirely of trigeminal fibers. A part of the nerve fibers leading from a group of ganglion cells could always be traced to nervus terminalis branches and in most cases all of the nerve fibers associated with a group of ganglion cells could be traced to nervus terminalis origin. It seemed to us desirable to determine even approximately the number and distribution of the ganglion cells associated with the nervus terminalis.
TABLE 1
birth ... \ Ha R 158 127 455 174 914 f A L 130 220 153 173 676 1 day after birth -\ B R 120 205 132 166 624 r A L 166 144 86 161 557 6 days after birth ...{ A R 93 139 117 119 468
1 The vomeronasal cartilage was taken as the line of division between course and distribution of the vomeronasal nerve.
2 The first four numbers of this column no doubt include sheath cells in the count.
The results obtained are collated in the accompanying table. For the two older stages the number of ganglion cells as given appears to us to present the facts fairly accurately, in that it was possible to differentiate between ganglion cells and sheath cells with relative certainty. In the counts attention was paid largely to the nuclei, and only cells in which the nuclei were evident in a given section were counted for that section. For the two younger stages the count is, we believe, relatively high, since in the compact masses, especially in ganglia found in the region of the vomeronasal organ, in which the cytomorphosis seems less complete, it was difficult to determine clearly between the nuclei of ganglion cells and the sheath cells. A certain degree of uniformity will be noted in the figures presented for the two older stages. The figures given for .the two younger stages for corresponding regions are throughout somewhat higher than for the two older stages. Especially is this noticeable in the column headed, "On the distribution of the nerves about the vomeronasal organ." In the two younger stages, as was noted, it was difficult in this region to differentiate clearly between sheath cells and ganglion cells, while in the other regions this differentiation was more readily made. In the material at our disposal it is not possible to determine definitely and finally the character of the neurones composing the numerous small ganglia associated with the nervus terminalis. The evidence at hand is negative rather than positive. Throughout the several series the peripheral nerves are well stained. The cell bodies of the neurones are stained various shades of brown, the nuclei appearing as lighter or again as darker areas in the cytoplasm, often distinctly circumscribed. Many of the nerve cells present distinct evidence of a neurofibrillar network in the cytoplasm. The cell outline, however, is not always as distinctly and definitely brought to view as could be desired. The neurones of the sensory ganglia of the cranial nerves are throughout our series differentiated with distinct outline and sharply demarked processes. A want of distinct differentiation is on the whole also noted for the cranial autonomic ganglia. In the sphenopalatine ganglion of our series, the neurones are not distinctly outlined and their processes are not clearly brought to view. In figure 2, we have presented, for comparison, a group of detail figures comprising clusters of ganglion cells associated with a septal branch of the nervus terminalis, situated anterior to the path of the vomeronasal nerves, and small but characteristic areas taken from the Gasserian ganglia of the corresponding series. The nervus terminalis ganglia, one for each stage of our series, are arranged in vertical column to the left of the figure, placed chronologically, A to D, and designated by lower case 'a'. The areas taken from the Gasserian ganglion of each of the respective stages of our series are chronologically arranged in vertical column to the right of the figure, and designated by a lower case '&.'
A glance at Fig. 2 Groups of ganglion colls of nervus terminalis and portions of the Gasserian ganglion from each of the stages of rabbit embryos and young rabbits used in this study. A, rabbit embryo, 3 cm. crown-breech length; B, rabbit embryo about one week before birth; C, young rabbit one day old; D, young rabbit six days old: «, ganglion cell groups taken from septal distribution of nervus terminalis. anterior to the path of the vomeronasal nerves; b, portions of the Gasserian ganglion. Pvridine-silver stain. X 200. the figure will show the distinct difference in the form and grouping of the nerve cells shown in the figures comprising the two columns. In column a, there are no distinct processes to the nerve cells and these are grouped around relatively fine nerve fibers. In column b, a progressive metamorphosis, characteristic for developing peripheral sensory or afferent neurones is noted. In A, b, from the Gasserian ganglion of a 3 cm. rabbit embryo the nerve cells are distinctly bipolar; in B, b, certain of the cells are unipolar with a short single process, presenting Yshaped or T-shaped divisions; in C and D, b, neurones with long single processes dividing into central and peripheral branches as characteristic of afferent or sensory neurones, are evident. The series of figures A to D, a, present a structure which is very similar to that shown by the sphenopalatine and ciliary ganglia of the corresponding stages, as shown in our series. Even in the two older stages of our series, fixed by means of preliminary ammoniated acohol injection, the processes of the neurones of the autonomic cranial ganglia are not clearly brought to view. The statements here made relative to the ganglion cell groups found in connection with the septal portion of the nervus terminalis are equally pertinent when applied to the ganglion cell groups of its intracranial portion. In not one instance were we able to observe nerve cells, found in relation with the intracranial portion of the nervus terminalis of the rabbit, even in the 'ganglion terminale,' which presented clearly the characteristics of peripheral sensory or afferent neurones; and this in material in which the neurones of the sensory cranial ganglia were well characterized. In figure 3, we present the very few instances in which neurones found in connection with the terminalis were distinctly stained, not the jet black of the ordinary chrom-silver preparations, as the figure would lead one to assume, but of a dark brown color with processes clearly brought to view. Cells a, 6, and c of figure 3, are from the intracranial portion of the terminalis of a oneday-old rabbit. Cell d, of this figure is taken from a small group of ganglion cells found in connection with the septal portion of the terminalis of a rabbit, six days old. The nerve cells here shown present the morphologic characteristics of sympathetic neurones and are regarded as such. In e, of figure 3, is shown the one instance observed of a structure resembling a pericellular ending of a white ramus or preganglionic fiber in a sympathetic ganglion. This was observed at one edge of a small group of ganglion cells in the immediate vicinity of the 'ganglion terminate' of a one-day-old rabbit. It is sketched at a much higher magnification than are the nerve cells of the same figure. The coil complex appears too small to enclose the cell body of a sympathetic neurone, judging from adjacent nerve cells. We may dismiss this structure with the statement that its appearance suggests a pericellular ending of a white ramus or preganglionic fiber characteristic for sympathetic ganglia. Fig. 3 Types of ganglion cells found in the course of the nervus terminalis, pyridine-silver staining; a, b, c, cells taken from the intracranial portion of a rabbit one day old; d, from septal portion of a rabbit six days old. X 200. e, a structure resembling a pericellular basket, the ending of a preganglionic nerve fiber, from the ganglion cell group of the intracranial portion of the nervus terminalis of a rabbit one day old. X 300. As concerns the ultimate terminations of the nervus terminalis, our material is not wholly adequate to enable us to draw definite conclusions. We have been able to trace terminalis branches to certain blood vessels of the septal mucosa, but their ultimate endings have not been clearly determined. We are, therefore, not in a position to state whether such endings are to be regarded as of the type of free sensory endings distributed to the adventitial coat or motor endings distributed to the muscular coat. Terminalis branches in the older stages, especially in the six-day stage, have been traced to the ducts of septal glands, less clearly to the gland alveoli. Here also the ultimate endings have not been clearly defined. Ultimate terminalis branches have not been traced with certainty to the epithelium of the olfactory mucosa, although fine terminal nerve branches which are independent of the special sense cells, such as are described by authors, have been observed in the olfactory epithelium, especially that of the vomeronasal organ. As previously noted, terminal nerve filaments which were traced to trigeminal branches commingle here and there with the end filaments of the terminalis and this renders it difficult to speak with certainty concerning the ultimate distribution of the nervus terminalis. A brief review of the literature dealing with the nervus terminalis of mammalia, and considered in the light of our investigations, may here be permitted. We have previously noted the work of Johnston and McCotter. To the references made the following may be added: Johnston's observations were made largely on sections of mammalian embryos, not stained with differential nerve stains. The Golgi method was used on pig embryos and an impregnation of the peripheral fibers obtained and the distribution of the terminalis to the vomeronasal organ verified. Whether a differential staining of the terminalis fibers was obtained is not stated. A few bipolar cells connected with its fibers were stained by the Golgi method. Extracranial ganglion cells were apparently not observed In the human embryos studied, a distinct ganglion terminale was noted and it is stated, "that the nervus terminalis joins with numerous strands of the olfactory nerve to make up the network of nerve bundles in the septum nasale." In the rabbit, as noted, the main septal branches of the terminalis are situated in a deeper plane in the mucosa than are the olfactory strands, and except for branches following the vomeronasal nerves, cannot be regarded as accompanying the olfactory nerves. We have not observed bipolar ganglion cells in the ganglion terminale nor in the more peripherally placed ganglia, and in our preparations these ganglion cells do not resemble peripheral sensory cerebro-spinal cells. McCotter has observed the intracranial portion of the nervus terminalis in adult dogs and cats with a ganglion terminale, and has traced it to its connection with the forebrain and the vomeronasal nerve. The methods used do not seem to admit of differentiation of terminalis and vomeronasal fiber, after these have joined. The fact that ganglion cells were found attached to the vomeronasal nerve just dorsal to the vomeronasal organ leads him to conclude that filaments of the terminalis " extend into the nasal cavity along with several filaments of the vomeronasal nerves and apparently terminate within or very close to the vomeronasal organ." This our preparations demonstrate conclusively for the rabbit.
Two other observers have dealt with the nervus terminalis of mammalia, namely DeVries and Dollken. The observations of DeVries extend to human and Guinea pig embryos. His results require but brief consideration, since, as agreed by authors who have reviewed his work, DeVries regards the nervus terminalis and the vomeronasal nerve as equivalent to the nervus terminalis of fishes, and believes that a similar structure is to be found in the whole vertebrate series. He recognized the vomeronasal nerve and the ganglion terminale or the vomeronasal ganglion, with a root entering the rhinencephalon on the mesial side of the olfactory lobe caudal to the olfactory bulb. Dollken had at his. disposal an abundant material, consisting of mouse, rabbit, Guinea pig, pig an human embryos. His investigation is concerned largely with the central connections of the nervus terminalis. So far as concerns his observations on the peripheral distribution of this nerve we are convinced that he is dealing not only with the nervus terminalis but has included also the vomeronasal nerve. This Johnston has recognized. Dollken uses as synonyms the words 'ganglion terminale,' 'ganglion nasale,' 'ganglion vomeronasal' and 'Nebenbulbus,' and his statements concerning the peripheral branches of the terminalis, in all of the forms studied, lead us to believe that he has not differentiated between vomeronasal nerve and terminalis, regarding the latter as a special nerve to the vomeronasal organ. His text figures, 4, 5, and 6, given to illustrate the peripheral distribution of the terminalis and its relation to the vomeronasal organ and the ganglion terminale, as observed in rabbit embryos, which we are able to compare directly to our own, made this very clear to us. A comparison of text figure 6, rabbit embryo of 28 mm. with our youngest stage, rabbit embryo 3 cm. in which the nervus terminalis is differentially stained and can thus be clearly separated from the vomeronasal nerves, makes this confusion very evident. This observer describes for mouse embryos, numerous cells which he regards as nerve cells, in connection with the peripheral distribution of the terminals. I older stages in the course of the nerve only relatively few ganglion cells were observed. He states that the appearances presented seem to indicate that these cells are only necessary to further the growth of the nerve. One may presume, he adds, that the ganglion cells are nutritive organs, subserving the growth of the fibers to the sense cells and the centrally placed nerve cells, the nerve cells after completion of their function undergoing regression, their fibrillae forming other relations in the course of the nerves. In the rabbit also, the ganglion cells found in the course of the nervus terminalis are said to show regression as development proceeds. Our observations on the rabbit, and especially such as pertain to older stages than those 1 studied by Dollken, warrant the statement, that there is no material reduction in the number of ganglion cells found in connection with the terminalis as development proceeds. In a human embryo of 21 mm. crown-breech length and in an older stage, presumably 35 mm. crown-breech length, Dollken observed numerous cells in the ganglion terminale which, after silver impregnation, showed great resemblance to the cells of the intervertebral and head ganglia, and which were apparently further developed than were the cells of the Gasserian ganglion. As stated by Johnston, Dollken "has failed to recognize the clear distinction which exists between ganglion terminale and the cells lying along the olfactory nerve fibers ('olfactory ganglion') which later produce neurilemma cells," and with this we agree. In all of our preparations of rabbit material there is evident a distinct difference in the form and the relations of the ganglion cells of the nervus terminalis and of those of the Gasserian ganglion. Since Dollken has not differentiated between the fibers of the nervus terminalis and vomeronasal nerve fibers his statements concerning the ultimate distribution of the terminalis fibers must be interpreted with this fact in view. We have not in our preparations, with differentially stained terminalis fibers, been able to trace with certainty ending of these fibers into the epithelium of the vomeronasal organ, and are thus disposed to regard the fine nerve fibers found in the olfactory epithelium and not connected with the special sense cells as very probably, in part at least, of trigeminal origin. As concerns Dollken's observations on the central origin of the nervus terminalis we may state that we have not observed the four roots of entrance as described by him. His root V corresponds closely with the main terminalis root as observed by us, in this we agree with Johnston. The small root entering more dorsally, as noted by us, may correspond with Dollken's root 'a'. The other roots we have not observed. The literature dealing with the nervus terminalis of vertebrates other than mammalia requires but brief consideration, since it has been dealt with in several of the recent contributions and since in the majority of the studies stress is laid on the central connections rather than on the peripheral distribution, which was not always clearly followed. For reptilian embryos Johnston has described groups of ganglon cells found at intervals along the dorsal division of the olfactory nerve, which he attributes to nervus terminalis. An instance in which ganglion cells are found on the peripheral portion of this nerve. It is a question in our minds as to whether the olfactory ganglion, a part of the trigeminal complex as described by Rubaschkin for chick embryos, is to be considered as related to the terminalis. This olfactory ganglion is described as lying under the dorsal and caudal portion of the olfactory mucous membrane and contains in the main bipolar cells, with peripheral processes traced into fine filaments which end in the olfactory epithelium and central processes traced to the Gasserian ganglion. Further observations made in the light of more recent investigations, seem necessary before the relations of the 'olfactory ganglion' to the ganglion terminale can be determined. Of the more recent contributions dealing with the nervus ternvnalis in amphibia and fishes, the following may be mentioned briefly. Herrick, in the frog, was unable to trace terminalis fibers further than " 1 mm. beyond olfactory bulbs." Accordingly he does not assign a distribution although he assumes that it accompanies olfactory strands, since ganglion cells are found scattered along the course of some of the latter. McKibben, in urodele amphibia, was able to follow the nervus terminalis only some 2 mm. distal to its superficial origin, and thus does not give its distribution. Sheldon, in the carp, states that terminalis fibers "are distributed to the epithelium with olfactory fibers." Brookover, for Amia and Brookover and Jackson, for Amieurus, give the peripheral distribution as associated with the olfactory strands. Sewertzoff reports that in Ceratodus forsteri, the distribution is to the anterior part of the nasal cavity and to the ordinary, not olfactory epithelium, and is decidedly of the opinion that it " does not serve an olfactory function." In this he is quite at variance with the conclusions of Brookover who regards the nervus terminalis as a component of the olfactory nerves. Brookover and Jackson reach the same conclusion regarding the nerve in Amieurus, basing their opinion on embryologic evidence. The majority of authors dealing with the nervus terminalis appear to have regarded it as an afferent nerve, homologous with the cutaneous sensory nerves of other regions. Brookover suggests that it may be of vasomotor function, and Brookover and Jackson express the same opinion, although in both articles it is admitted that there is no definite evidence. The evidence given by Brookover for connecting the nervus terminalis to the post optic sympathetic system by way of the intracranial sympathetic system, which he described, seems insufficient to us to establish this connection. We quote his summary of the evidence : "The nature of the Golgi impregnation on which I have had to depend to a large extent for tracing these intracranial fibers does not permit of demonstrating the connections between the nervus terminalis and the posterior portion of the sympathetic as clearly as would be the case with medullated fibers by the Weigert method, but the slightly diminished bundle of fibers of fig. 22 (intracranial sympathetic, our insertion) certainly continues rostral along the carotid artery beneath the olfactory nerve, while the fibers of the nervus terminalis just as certainly become more or less distinctly separated from the olfactory nerve, after it enters the cranial cavity, and run near the same artery." In certain of our series we find small bundles of nerve fibers, such as he describes accompanying the various intracranial blood vessels situated under the anterior part of the brain and olfactory bulbs, and passing in very close proximity to nervus terminalis strands without observing any anastomosis of nerve fiber bundles of the respective systems. We consider, therefore, that in order to establish a connection in this region it is necessary to show an actual fiber continuity, not a mere proximity. After thus considering briefly the literature, we may proceed to our own conclusions.
Our observations on the nervus terminalis of the rabbit warrant, we believe, the following statements: By reason of the differential staining of the nervus terminalis, in all of the stages of our series, we conclude that this nerve is not a component part of the olfactory and vomeronasal complex, but an independent nerve, with central connections by means of several small roots to the ventro-mesial and mesial portion of the forebrain, caudal and independent of the olfactory stalk, and courses in the form of a loose plexus along the ventro-mesial surface of the olfactory bulb, reaching the nasal septum on the mesial surface of the vomeronasal nerve, which nerve it follows to the mucosa of the vomeronasal organ, and is further distributed to the septal mucosa anterior to the path of the vomeronasal nerve, in which region especially it is joined by terminal branches of the trigeminus, mainly from the nasopalatine branches. In the course of this nerve, even in connection with its more peripheral branches and beginning with its intracranial portion, there are found numerous smaller and larger groups of ganglion cells. One of these groups, of relatively larger size than the other, is situated on its intracranial portion in the region where the terminalis approaches the vomeronasal nerve. This larger group is regarded by us as the ganglion terminale of authors. The groups of ganglion cells found in the course of the nervus terminalis of the rabbit present the appearance of small sympathetic ganglia, similar in general structure and appearances to cranial autonomic or sympathetic ganglia found in our series, and differing in form and arrangement of neurones from those of the intervertebral and cranial afferent sensory ganglia of the respective series. The nerve fibers of the terminalis have more the appearance of sympathetic and preganglionic fibers than of neuraxes or dendrites of sensory neurones. Distribution of ultimate terminalis branches to blood vessels and glands of the septal mucosa seems probable, though this we cannot assert positively since the commingling of trigeminus and terminalis terminal filaments has been observed.
For the present we reserve definite statement as to the probable function of the nervus terminalis of the rabbit, realizing fully that further work with the introduction of other methods is necessary. If we consider only the peripheral distribution of the nerve, the size of its component fibers, its arrangement in loose plexus, character, number and disposition of associated ganglion cell groups, we should favor ascribing to it an autonomic function. Its central connection, however, both in character and place of origin, does not wholly conform with our conception of deep and superficial origin of the preganglionic nerve fibers of a sympathetic path. BIBLIOGRAPHY The literature here listed does not include nearly all of the contributions dealing with the nervus terminalis and olfactory and vomeronasal nerves which have been consulted. The literature dealing with the nervus terminalis in mammalia is included, and of the other papers only the more recent and pertinent ones.
Brookover, Charles 1910 The olfactory nerves, the nervus terminalis and the preoptic sympathetic system in Amia calva. Jour. Comp. Neur., vol. 20. Brookover, Charles, axd Jackson, T. S. 1911 Olfactory nerve and nervus terminalis of Amieurus. Jour. Comp. Neur., vol. 21. DeVries, E. 1905 Note on the ganglion vomeronasale. K. Akad. van Weten schappen te Amsterdam, vol. 7. Dollken, A. 1909 Ursprung und Zentren des Nervus Terminalis. Monatsch. f. Psych, u. Neur. Bd. 26, Ergenz. Heft, Herrick, C. Jtjdson 1909 The nervus terminalis in the frog. Jour. Comp. Neur., vol. 19. Johnston, J. B. 1913 The nervus terminalis in reptiles and mammals. Jour. Comp. Neur., vol. 23. McCotter, R. E. 1913 The nervus terminalis in adult dog and cat. Jour. Comp. Neur., vol. 23. McKibben, Paul S. 1911 The nervus terminalis in urodele amphibia. Jour. Comp. Neur. vol. 21. Rubaschkin, W. 1903 Uber die Beziehungen des Nervus Trigeminus zur Riech schleimhaut. Anat. Anz., Bd. 22. Sewertzoff, A. N. 1902 Zur Entwickelungsgeschichte des Ceratodus forsteri. Anat. Anz., Bd. 21. Sheldon, R. E. 1909 The nervus terminalis in the carp. Jour. Comp. Neur., vol. 19.
THE ATRIO- VENTRICULAR CONNECTION IN THE REPTILES HENRY LAURENS
Sheffield Biological Laboratory, Yale University SEVEN FIGURES In connection with some physiological experiments on the coordination of the reptile heart and its disturbance (Laurens '13), I have undertaken an histological examination of the hearts of these animals with particular reference to the atrio-ventricular connection and should like to report briefly the results of this investigation. Such an histological study seemed necessary not only as supplementary to the physiological experiments but also owing to the contradictory views which are expressed about this region of the reptile heart. On looking over the literature dealing with the anatomy of the tortoise and lizard hearts one is struck by the lack of accurate and clear accounts of the connection of one part of the heart with another, as well as of the distribution of the nervous elements in the heart. This is true for the tortoise, but much more so for the lizard. In the case of the latter one finds the contradictory views of Imchanitzky, that there is no muscular connection between the atria and the ventricle, and of Kulbs and Lange, that the heart of the lizard consists of four parts which are connected muscularly. Again, while Imchanitzky describes a nerve plexus with very large and small ganglion cells, by means of which the auricles are connected with the ventricle, Kiilbs and Lange have never found nerves and ganglion cells in their muscular atrioventricular connection. In the paper referred to the literature dealing with the anatomy of the atrio-ventricular connection in the reptiles was reviewed in 273 274 HENRY LAURENS full, so that there is no need to do so again. 1 The conclusion which is to be derived from a reading of this literature was there stated, (p. 148) and is, that between the auricles and ventricle of the reptile heart a muscular connection undoubtedly does exist. The results of Dogiel ('07) and Imchanitzky ('09) however, stand in direct opposition to this view. According to them, the different parts of the heart are not connected muscularly, and the connection between the auricles and ventricle is effected solely by means of a large nerve bundle which runs in a band of connective tissue on the dorsal side of the heart. Dogiel called this band of tissue the 'Ligamentum Atrioventriculare.' The same species of lizards (L. viridis and agilis) and of tortoise, (Clemmys lutaria) as were used for the physiological experiments have been examined histologically. In addition, the hearts of the sculptured tortoise (Chelopus insculptus) and of the common box tortoise, (Cistudo Carolina) and one heart of a snake, (Storeria dekayi) have also been studied. The hearts were fixed in Flemming's strong solution or in concentrated corrosive sublimate, imbedded in paraffin and sectioned, 5 to 7 n in the case of the lizards and 10 to 15 /x in the case of the tortoises. For staining, Heidenhain's iron hematoxylin, followed, after differentiation, by van Gieson's picrosaurefuchsin mixture was used and gave excellent results. By this method a beautiful differentiation between muscular and connective tissue is obtained and the striated musculature is finely shown. Good accounts of the general anatomy and histology of the different parts of the lizard and tortoise hearts will be found in the literature referred to. I wish to give only a brief description of the connection between the auricles and the ventricle — the atrio-ventricular funnel — and of the intra-cardial nervous system as far as I have been able to carry out this part of the work. The atrio-ventricular connection in the lizard and tortoise hearts may be described together, since in the species examined by me 1 The work by Greil, which was unknown to me at the time, should be here mentioned. Greil speaks of and figures, though he does not describe in any detail, an 'Aurikular' or 'Atrio-ventrikularring' of musculature, by means of which the auricles and ventricles of various reptiles including the lizard and tortoise, were connected. ATRIO- VENTRICULAR CONNECTION: REPTILES 275 the conditions, as far as I have been able to make out, are identical. The drawings, which were made with the aid of the camera lucida, are all of the lizard heart, (L. agilis.) In frontal and sagittal sections, (figs. 1, 2 and 3), the auricles, separated by the septum, can be seen to extend downward in the form of a closed tube, which is more or less funnel shaped, into the cavity of the ventricle. A cross-section (fig. 4) through the base of the ventricle, a little below the level at which the septum goes over into the atrio-ventricular valves, shows the atrio-ventricular funnel to be a closed ring, clearly separated from the ventricle by a fairly thick layer of connective tissue, in which numerous blood vessels and ganglion cells are to be seen. As the funnel extends farther into the ventricular cavity it approaches nearer and nearer to the ventricle, at the same time becoming thinner, particularly on the dorsal side. The connective tissue between the funnel and the ventricle also becomes less in amount and finally the two kinds of musculature are in direct contact. In a cross section (fig. 5.) through the ventricle, nearer the apex, and at a level a little below that represented by the linea.v.v. in figure 2, it is seen that the funnel of musculature is no longer in the form of a closed ring, but that it is now interrupted on the ventral side by the vessels of the bulbus with the walls of which it becomes connected. At about the same level on the dorsal side the funnel musculature has become directly connected with that of the ventricle. Thinning out gradually, it can be seen to go over into that of the ventricle. From this first dorsal place of connection the junction of the two forms of musculature spreads to the right and to the left, and the last parts of the funnel to become connected with the ventricle are the two sides, right and left (fig. 6) and of these the left extends further into the ventricle, than does the right. A part of the original funnel on the left ventral side (fig. 6) persists for a considerable time after all the remainder has disappeared, and finally becomes connected with the inner wall of the ventricle. The musculature of the funnel goes over directly into that of the ventricle. The fibers of the funnel are arranged circularly, and there is a good deal of connective tissue in among them as a.v.f. Figs. 1 to 7 All the figures are of the lizard heart (Lacerta agilis) and were drawn with the aid of the camera lucida. Fig 1 Frontal section through the whole heart at a level slightly ventral to the horizontal median line; a.v.f., atrio-ventricular funnel; a.v.v., atrioventricular valve; La., left auricle; r.a., right auricle; s.a., septum atnorum. X 20. . Fi- 2 Sagittal section through the right side of the heart; a.v.f., atrio-ventncular funnel; a.v.v., atrio-ventricular valve; d.L, dorsal ligament; r.a., right auricle; s., part of the sinus venosus. X 20. Fig 3 Sagittal section through the left side of the heart just median to the entrance of the pulmonary vein; a.v.f., atrio-ventricular funnel; a.v.v., atrio-ventricular valve; p.v., pulmonary vein; s.a., septum atnorum. X -0. 276 ATRIOVENTRICULAR CONNECTION I REPTILES 277 well as numerous capillaries. The funnel musculature can easily be distinguished from that of the ventricle on account of its brighter appearance, as it does not stain so deeply. Differences in the striation of the muscle fibers and in the size and shape of a.v.f. a.v.f Fig. 4 Cross section through the ventricle just below the atrioventricular groove; a.v.f., atrio-ventricular funnel; a.v.v., atrio-ventricular valve; b., bulbus; c.t., connective tissue. X 40. Fig. 5 Cross section through the ventricle nearer the apex than in figure 4 and at about the level represented by the line a.v.v. in figure 2; a.v.f., atrio-ventricular funnel; a.v.v., atrio-ventricular valve; b, vulvus; v., ventricle. X 40. the nuclei are also apparent. The fibers and nuclei of the muscle cells of the funnel are similar to those of the auricles. The striation is very distinct but fine, and the nuclei are large and round or slightly oval. The ventricular fibers are more coarsely stri 278 HENRY LAURENS ated, and the nuclei are long and narrow. Further, the muscle fibers of the funnel and of the ventricle run in different directions, so that there is little difficulty in distinguishing the two. The smooth muscle cells described by Bottazzi ('07) as occurring in the auricles of the tortoise, Emys europaea, are seen very clearly in the auricles of all the tortoises that I have examined. They occur, as Bottazzi described them (p. 171), as a layer immediately under the endothelium of the auricles and are a continuation of the tunica media of the large veins. I have not been able to follow them into the ventricle. Oinuma ('10) has recently referred the oscillations in tone of the auricles of the tortoise, as well as the lasting increase in tonus, to the activities of this smooth musculature. In earlier investigations Bottazzi ('97) could not find any trace of these variations in tone in the auricles of several batrachian and reptilian hearts, one of which was the lizard, Lacerta viridis. I also could never see these variations in tone in the auricles of the lizard and have looked in vain for the presence of smooth muscle cells in the auricles of both L. viridis and agilis. The connection which Dogiel and Imchanitzky describe as existing between the auricles and ventricle of the tortoise and lizard has been shown to have absolutely no significance for the co-ordination of the heart (Laurens '13, pp. 144 and 159). Since it is claimed by these authors to be the sole means of connection between the auricles and the ventricle, I have studied it carefully both in the pulsating heart and in sections. On the dorsal side of all the lizard and tortoise hearts that I have examined there is to be seen a direct connection, which I have called the dorsal ligament, between the sinus and the ventricle. It is well over to the right side (figs. 2 and 7) and appears as a broad, flat band in which, under the binocular, nerves and blood vessels can be seen. The coronary vein and the 'coronary nerve' or nerves (Gaskell) do not run free, but in this band of tissue, which is a fold of the pericardium. In sections, the band, or dorsal ligament, is seen to be made up of connective tissue which begins at the sinus venosus ATRIO- VENTRICULAR CONNECTION: REPTILES 279 and runs superficially over the auricles and the auriculo-ventricular groove to end on the dorsal surface of the ventricle. Along its course are found several collections of ganglion cells and blood a.v.f. Fig. 6 Cross section through the ventricle below the level of theatrio-ventricular valves, a.v.f., atrio-ventricular funnel; b., bulbus. X 40. Fig. 7 Dorsal view of the heart to show the nerves; a.v.v., atrio-ventricular valve; c.n., the 'coronary nerve;' d.l., the dorsal ligament; p.v., the pulmonary vein; s., the sinus venosus; s.a., the septem atriorum. vessels. It therefore does not connect the auricles with the ventricle, as Dogiel and Imchanitzky claim, but is a pathway between the sinus and the ventricle for nerves and blood vessels. 280 HENRY LAURENS The innervation and intracardial nervous system of the reptile heart has been described by a number of investigators. I have succeeded in staining the intracardial nervous system of the isolated lizard heart by means of methylen blue. Owing to the difficulty of obtaining material at the time of year at which my observations were made they have not been carried very far. It is my intention to continue this work and to make a detailed study of the intracardial nervous system of the lizard. The preparations which I have made show the auriculo-ventricular funnel richly supplied with nerves, contrary to the opinion of Kulbs and Lange, and have convinced me that a separation of the nerves and musculature of this connection are hardly any more possible in the lizard heart than in that of any other vertebrate. In my material fixed in Flemming's solution and corrosive sublimate the ganglion cells are very well preserved and the account of the intracardial nervous system is in part taken from sections of these hearts. The lizard heart (L. viridis and agilis) (see fig. 7) is supplied by two nerves, which, according to Kiilbs and Lange, are branches of the vagi, the left -nerve supplying the most of the heart. The right divides just cephalad of the heart into two branches, the one passing to the dorsal, the other to the ventral side and supplying the bulbus. The dorsal branch runs to the sinus, fine branches ramifying over its walls and other small branches supplying the right auricle. A large branch runs directly from the sinus to the ventricle along the dorsal ligament. This branch can be called the 'coronary nerve' since it corresponds to the nerve of that name in the tortoise heart. All along its course are found ganglion cells, which decrease in number as the ventricle is approached. This nerve does not enter the auriculoventricular groove, as Gaskell describes for the tortoise, a condition which I have also not been able to verify in that animal, but spreads out over the dorsal surface of the ventricle. The left nerve has a larger surface to supply. It gives off first a large branch which enters to the median side of the single pulmonary nerve, where, in sections a very large ganglionic mass can be seen, which almost surrounds the opening of the vein into the left auricle. The main branch of the left nerve enters the heart ATRIOVENTRICULAR CONNECTION! REPTILES 281 at the opening of the sinus to the right auricle where again in sections a large collection of ganglion cells is seen. Previous to entering the heart it gives off a small branch which enters the right auricle near the beginning of the septum and runs along it with ganglia in its course. From the main branch there are also several other branches given off which ramify over the dorsal wall of the left auricle and, crossing the auriculo- ventricular groove, pass to the ventricle (fig. 7) . From the examination of the sections, several collections of nerve cells are to be seen. The largest and most conspicuous of these are two at, or around, the entrances of the veins into the auricles. In the dorsal ligament the nerve cells are very numerous and often aggregated into masses of eight to ten cells each. In the connective tissue of the auriculo-ventricular groove numerous scattered nerve cells are seen, sometimes very closely in connection with the funnel musculature. In the septum atriorum there are two ganglionic masses, the first near the beginning of the septum, the other very near the atrio-ventricular valves. In the auriculo-ventricular funnel ganglion cells seem to be scarce, and I have seen them scattered only here and there, and chiefly on the ventral side. I have not been able to see ganglion cells in the musculature of the ventricle and of the bulbus. Imchanitzky, using methylen blue, has been able to demonstrate nerve cells through the whole ventricle, they being most numerous in the neighborhood of the bulbus aortae. In the tortoise nerves can be seen running along the superior venae cavae to the heart. On the right side it can be seen that a branch ('coronary nerve') runs directly from the sinus under the vein to the ventricle, the remainder of this nerve being distributed to the sinus, and perhaps a small branch to the right auricle. The nerve on the left side is distributed principally to the left auricle from which can be made out several branches which run to the ventricle along the auriculo-ventricular groove, some ending here and others continuing on to the dorsal surface of the ventricle. Running to the ventral side of the heart are several fine branches which divide and are distributed to the different vessels of the bulbus aortae. 282 HENRY LAURENS Groups of ganglia are more numerous in the tortoise heart than in that of the lizard. The largest are again two at the opening of the sinus and of the pulmonary veins into the auricles. In the dorsal ligament there are numerous groups of ganglia all along the course of the 'coronary nerve.' On the dorsal side of the left auricle, just under the pericardium there are numerous small groups of ganglia to be seen, some consisting of only two or three cells. At the beginning of the septum atriorum, on the right side, there is a collection of ganglia and also several small groups of nerve cells along this side of the septum. In the connective tissue of the auriculo-ventricular groove, particularly on the left side, and in the connective tissue in the proximity of the bulbus, the ganglionic masses are very numerous, though small, consisting of from two to five cells. When traced through the sections the nerve cells in the connective tissue of the auriculoventricular groove are seen to be connected with those of the bulbus. It was found from physiological experiments (Laurens '13, p. 176) that in the reptile heart there is a certain amount of differentiation in the atrio-ventricular conduction paths. The right and left sides of the atrio-ventricular funnel were found to have the power of retaining co-ordinated the sequence of ventricular upon auricular beat when other parts of the connection were cut away. The left ventral side seemed more important than the right in preserving this co-ordination. These physiological results stand in accord with those obtained from histological examination. As has been pointed out the auricles and ventricle are connected by a muscular funnel which extends down from the auricles into the cavity of the ventricle and becomes connected with its musculature. There is no such 'ring' as Gaskell describes, and the two kinds of musculature go over directly into one another. The fibers of the funnel are arranged circularly, but this arrangement can in no way be regarded as a well defined ring in the sense in which Gaskell used it. ATRIOVENTRICULAR CONNECTION! REPTILES 283 The differentiation in function of the atrio-ventricular connection can, I believe, be explained in the light of the structural conditions. Gaskell ('84, p. 67) described a certain part of the muscular connection which had more than any other part the property of preserving the co-ordination between the auricular and ventricular beat when the remaining portions were cut away. This part was on the right ventral side under the aorta. Kiilbs ('12) explains Gaskell 's results on the assumption that there is found the direct connection between the auricular and the bulbils musculature. A slightly different explanation seems to me to fit the case better than the one suggested by Kulbs. As Keith and Flack ('07) have emphasized, the muscular atrioventricular connection in the reptiles is, in cross section, a ring, extending completely around the atrio-ventricular ostium, but in which there is evidence of concentration in that the tissue is more abundant at certain points than at others. The more recent investigations of Keith and Mackenzie ('10) corroborate this opinion. In cross sections of the lizard heart it is seen that there is evidence of concentration in that the musculature of the atrio-ventricular connection is thickest on the ventral side and to the right and left, and thinned out on the median dorsal side. When sections nearer the apex of the ventricle are examined (figs. 5-6) it is seen that it is the right dorsal and left ventral sides which are thicker than any other part. As has been pointed out, these are the parts of the atrio-ventricular funnel which are most intimately connected with the ventricular musculature, and in this fact, in my opinion, is to be found the explanation of the greater power of this part of the connection to preserve the co-ordination of the heart-beat. The fibers of these bundles of musculature, and particularly the left one, extend further into the ventricular cavity than do any other parts of the original muscular funnel and joining gradually along their course with the ventricle they form a stronger connection between auricles and ventricle than elsewhere. From a glance at the sketches of lizards' hearts (Laurens '13) shown in figures 18, 27, and 38, and of the tortoise heart, figure 41, which were drawn under a 284 HENRY LAURENS binocular after the experiment for which they had been used, had been concluded, it will be seen that the bridge of tissue shown as the sole means of connection between auricle and ventricle corresponds very closely to that part of the funnel musculature represented to the right and left in figure 6. SUMMARY 1. The auricles and ventricle of the lizard and tortoise are connected muscularly. 2. The atrio-ventricular connection is in the form of a tube, which extends downward from the auricles and is pushed funnelshaped into the cavity of the ventricle, with the muscular walls of which it becomes directly connected. 3. The differentation in function of the atrio-ventricular funnel is in accord with the structural conditions, in that the right and left sides which show the greatest power of preserving the co-ordination extend more deeply into the ventricular cavity and are more intimately connected with its musculature than are any other parts of the funnel. 4. The dorsal ligament ('Ligamentum Atrioventriculare' of Dogiel), connects the sinus with the ventricle. Along it runs a branch of the right vagus, the 'coronary nerve' from the sinus to the ventricle. 5. The atrio-ventricular funnel is richly supplied with nerves. Ganglion cells are, however, scarce. LITERATURE CITED Bottazzi, F. 1897 The oscillations of the auricular tonus in the batrachian heart. Jour. Physiol., vol. 21, pp. 1-21. 1907 Richerche sulla musculatura cardiale dell' Emys europaea. Zeitschr. f. Allg. Physiol., Bd. 6, S. 140-194. Dogiel, J. 1907 Einige Daten zur Anatomie des Frosch- und Schildkrotenherzens. Arch. f. mikroskop. Anat., Bd. 70, S. 1-96. Gaskell, W. H. 1883 On the innervation of the heart with especial reference to the heart of the tortoise. Jour. Physiol., vol. 4, pp. 43-127. ATRIOVENTRICULAR CONNECTION: REPTILES 285 Greil, A. 1903 Beitrage zur vergleichenden Anatomic und Entwicklungsgeschichte des Herzcns und des Truncus arteriosus der Wirbelthieren. Morph. Jahrb., Bd. 31, S. 123-310. Imchanitzky, M. 1909 Die nervose Koordination der Vorhofe und Kammer des Eideehsenherzens. Arch. f. Anat. (und Physiol.), S. 117-136. Keith, A., and Flack, M. 1907 The form and nature of the muscular connections between the primary divisions of the vertebrate heart. Jour. Anat. and Physiol., vol. 41, pp. 172-189. Keith, A. and Mackenzie, Ivy 1910 Recenl researches on the anatomy of the heart. Lancet, vol. 1, pp. 101-103. KtiLBS 1912 liber das Reizleitungssystem bei Amphibien, Reptilien, und Vogeln. Zeitschr. f. exper. Pathol, und Therapie, Bd. 11, S. 51-68. Kulbs und Lange, W. 1910 Anatomische und experimentelle Untersuchungen iiber das Reizleitungssystem in Eidechsenherzen. Zeitschr. f. exper. Pathol, und Therapie, Bd. 8, S, 313-322. Laurens, H. 1913 Die Atrioventrikulare Erregungsleitung im Reptilienherzen und ihre Storungen. Pfltiger's Archiv., Bd. 1.50, S. 139-207. Oinuma, S. 1910 Beitrage zur Physiologie der Autonom innervierten Musculatur. III. tiber den Einfluss des Vagus und des Sympathicus auf die Tonusschwankungen der Vorhofe des Schildkrbtenherzens. Pfltiger's Archiv., Bd. 133, S. 500-518. THE ANATOMICAL RECORD, VOL. 7, NO. 8 ul ANATOMICAL OBSERVATIONS ON A LIPOMA SIMULATING DIRECT INGUINAL HERNIA FRANK E. BLAISDELL, SR. The Division of Anatomy of the Depart mmt of Medicine, Stanford University TWO FIGURES During class work while a dissection was being made of the inguinal regions of an adult male cadaver, for the purpose of studying the anatomy of inguinal hernia, a lipomatous development was found to exist, that arose from the subperitoneal tissue beneath the triangle of Hesselbach on the left side of the body. The growth had followed the course usually taken by a direct inguinal hernia in the lateral and inferior third of the triangle. Fatty herniae have been known since the earlier days of anatomical investigation, as will be seen by review of the literature. Those who have chiefly contributed to the subject are the following: Morgani (1), Pelletan (2), Scarpa (3), Sir Astley Cooper (4), Cloquet (5), Maunder (6), Paget (7) and Gascoyen (8), Annandale (9), Wernher (10), Gay (11), Butlin (12), Tillaux (13), Stonham (14), Hutchinson (15), Broca (16), Douglas (17), Imbert (18), and Shattock (19), in 1908-09, gave the results of his investigation u On normal tumor-like formations of fat in man and the lower animals." The normal disposition of adipose tissue in the body is an important factor in the study of the subject. Its vagaries of distribution and sites of predilection are well known at the present day, but the causes for development in localized areas are not known. The dissecting room is a fruitful field for their discovery and study. Their distribution in the regions of inguinal herniae may be summed up as follows : 2S7 THE ANATOMICAL, RECORD, VOL. 7, NO. 8 SEPTEMBER, 1913 288 FRANK E. BLAISDELL, SR. 1. Their development in the subperitoneal connective tissue about the abdominal inguinal ring and their subsequent descent through it, into and along the inguinal canal to emerge through the subcutaneous ring. 2. Their development within the spermatic cord itself at any point of its course within the canal after the convergence of its constituents at the abdominal ring, or after its emergence through the subcutaneous ring. 3. Their development within the inguinal canal about the cord, in the lateral, median or medial thirds of the canal, and their subsequent emergence at the subcutaneous ring. 4. Their development in the superficial fascia over the inguinal canal, subcutaneous ring, and cord before it reaches the scrotum. 5. Their development in the subperitoneal tissue beneath the triangle of Hesselbach and their subsequent emergence, by rupture or the yielding of structures in that area, so as to enter the inguinal canal and emerge through the subcutaneous ring. 6. Their development between the abdominal muscles about the inguinal canal and Hesselbach's triangle. 7. Their development in the prevesical space and appearance at the subcutaneous ring, as in a case reported by Imbert, where a lipoma presented by way of the middle inguinal fossa. 8. Origin from the subperitoneal fat in the iliac fossa has been observed several times by Prof. A. W. Meyer, though unreported. It is not the purpose of the present paper to consider the subject from a pathological standpoint, but to present it from the viewpoint of anatomy. The incentive for reporting the present facts is the observation made in the dissecting room on the case above mentioned, where a lipoma simulated direct inguinal hernia. The anatomical relations presented by the growth and contiguous structures were very clear and definite in that case. The instance also presents an opportunity for making some critical remarks on the anatomical terminology involved in the anatomy of direct inguinal hernia. ANATOMICAL OBSERVATIONS ON A LIPOMA 2S9 A X ATOMICAL CONSIDERATIONS Hesselbach's triangle is a space between the inguinal ligament inferiorly, the inferior epigastric artery laterally and the lateral edge of the rectus muscle medially. The dorsal boundary of the triangle is formed directly by the fascia transversalis, more deeply by the subperitoneal tissue and peritoneum. The ventral covering for the medial two-thirds is the so-called conjoined tendon, for the lateral and inferior one-third the cremasteric muscle and fascia which take the place of the conjoined tendon; while more superficially are the aponeurosis of the external oblique, superficial fascia and integument. The size of the triangle is subject to considerable variation, and as Cloquet states depends in extent upon the distance of the inferior epigastric artery from the symphysis pubis. It also varies with the development of the rectus muscle. Measurements of the boundaries of Hesselbach's triangle in four cadavers gave an average of 45 mm. for the base at the inguinal ligament; 55 mm. for the medial boundary and 65 mm. for the lateral boundary. The variation was not over 5 mm. and that was chiefly in the lateral and medial boundaries, depending upon the variation in the obliquity of the inferior epigastric artery. The aponeurosis of the abdominal muscles vary in their degree of uniformity of thickness, and consequently in the power of resistance. At times there is more or less equality in the distribution and arrangement of the structures and therefore approximately of equal strength throughout; at other times certain areas are relatively weak and deficient at certain points. Usually when well developed the aponeuroses are opaque; when poorly developed more or less translucent. These variations depending upon developmental and other conditions. The extremes of the development may be observed, on the one hand, in the well developed abdominal muscle of the athlete or of the laborer; on the other, in individuals of under development or of sedentary habits, and as is well known the anterior abdominal walls are occasionally so thin that the peristaltic movements of the intestines may be more or less visible through them. 290 FRANK E. BLAISDELL, SR. McMurrich in his description of the conjoined tendon in Piersol's Anatomy, describes that structure as follows: ( hving to the oblique direction of the canal (inguinal), that portion of the aponeurosis of the external oblique which is strengthened by the intercolumnar fibres, together with a portion of the internal oblique, form its anterior wall; while its posterior wall is formed by the aponeurosis of the transversalis, together with the more medial lower portion of that of the internal oblique, these two layers of fascia (aponeurosis) uniting in this region to form what is termed the conjoined tendon, which is attached to the body and superior ramus of the pubis, and medially is especially thickened to form a band, the falx inguinalis, firmly attached along its medial border to the tendon of the rectus. More laterally, where it forms the medial boundary of the internal abdominal ring, it is also thickened, forming the ligament of Hesselbach (ligamentum interfoveolare). Between these two thickenings the abdominal wall is weaker and maj r give way to internal pressure, permitting a hernia, .... spoken of as direct hernia. (Fig. 1). In two of the four cadavers examined the falx inguinalis (conjoined tendon) showed but little differentiation into three parts, and the so-called intermedial weak point was apparently as thick and strong as the lateral and medial parts. In one, there was evident thinning of the middle portion, while in the other there was marked differentiation into three parts, the middle portion being translucent and very deficient in the white fibers so noticable in the two first mentioned. In one cadaver also there was a difference between the two sides. The four cadavers used for study were of middle age and moderately emaciated. Barker (20) in his " Anatomical terminology," gives the BNA for the conjoined tendon as the falx (aponeurotica) inguinalis, which is to be considered the term for that structure in its entirety. Although this term was adopted by the Commission, it is evident that the conjoined tendon is not synonymous with the falx inguinalis. It is certain that the conjoined tendon may consist of three parts, namely: the falx inguinalis, ligamentum interfoveolare and an intermediate thinner or attenuated portion which has not a definite name, and which I have called the pars intermedia. ANATOMICAL OBSERVATIONS ON A LIPOMA 291 Since a part cannot be equal to the whole it is evident that if the BNA term is to be perpetuated it should be considered synonymous with conjoined tendon, and considered as being made up of three parts, namely: the pars tendinea, attached by its medial border to the lateral edge of the rectus; ligamentum interfoveolare and the intermediate or weaker portion— the pars intermedia (fig. 1). It is necessary to call attention to certain points in regard to the fascia transversalis which was first described by Sir Astley Cooper (4), and named by Cloquet (5), who in 1835 stated that ll P'f WllliS ft mgastrica it.; — H-ffll kli i !»' HI Pars intermedia Lig- interfoveolare 1 , lill . MiU //,'.». M interfoveolans Pars tendinea M transversalis
■ Lig. inguinale nguinalis conjoined tendon) Fig. 1 Dissection of the posterior surface of anterior abdominal wall, showing relations of conjoined tendon and its expansions to internal abdominal ring (modified from Piersol). the fascia transversalis in this region is sometimes composed of two aponeurotic laminae united at the posterior border of Poupart's ligament; the anterior arising from Poupart's ligament itself; the posterior being continuous with the fascia iliaca, which quits the iliacus internus muscle to be reflected upon the anterior parietes of the abdomen. These two laminae which ascend together between the transversalis and peritoneum, are easily separated on the outer side of the superior opening of the inguinal canal, but are intimately united around and on the inner side of this aperture. When these two layers are distinct, the posterior usually passes behind the rectus to the linea alba, but the ante 292 FRANK E. BLAISDELL, SR. rior is continuous with the outer edge of the rectus. The epigastric arterjr is found either in front or behind, and sometimes between the two layers. That these two layers are frequently met with is to be admitted. The fascia trans versalis is described by Piersol (21), Gray (22), Morris (23), and Cunningham (24) as lining the inner or deeper surface of the transversalis muscle. As a distinct structure it is directly continuous with fascia in the lumbar, diaphragmatic, inguinal, and pelvic regions and does not constitute the aponeurosis or tendon of the transversalis muscle as some authors have implied. ANATOMICAL DISCUSSION In discussing the anatomy of the inguinal region, Douglas states that "One may readily allow that the stronger the so-called thickened fascia transversalis of the groin, the less is any disposition to rupture present, but it must likewise be noted that if that structure be of unequal resisting power in different parts, such disposition to rupture is increased." In preparations examined by him, he recognized the three parts of the conjoined tendon, their relative strength and position, and laid emphasis upon the ligamentum interfoveolare as the medial boundary of the abdominal ring. He also observed in certain specimens exhibiting herniae, in which the protrusion did not appear to be very long standing, that these bands or ligaments were specially well marked and he thinks that one may justly suppose that the tendency to rupture is increased when the inequality of resisting power is great between them and the rest of the tendon. Thus, in the case of oblique inguinal hernia, that if the medial boundary of the deep ring be especially strong, the outer limit of the opening will, with more readiness be separated from it when increased intra-abdominal pressure bears upon it, and so the deep ring will be opened up. The medial boundary or pillar of the deep ring is a part of the transversalis tendon, and it becomes tense and resistant when drawn upon in the contraction of that muscle, and consequently this will slightly ANATOMICAL OBSERVATIONS ON A LIPOMA 293 separate the two sides of the deep ring. Such a state is brought about when the body is flexed on the thighs, or vice versa; when in the erect position of the body the two sides of the rings are approximated. Therefore taxis for the reduction of hernia is most effective when the thighs are flexed. In regard to direct inguinal hernia, he suggests that their production would be favored if the two bands alluded to were greatly stronger than the intervening tendon, and suggests that a fat hernia may be the cause of any inequality in the resisting power of the wall. It is logical and in keeping with facts that the pars intermedia, which is the weakest part of the falx inguinalis should be the point to give way, and the tenseness of the pars tendinea and ligamentum interfoveolare would only guide the protruding part and at the same time intensify the weakness of the pars intermedia by directing pressure to it. It is the intention to discuss the conditions leading up to the production of fatty inguinal or femoral herniae, only in so far as the direct form is concerned. REPORT OF A CASE OF LIPOMA SIMULATING DIRECT INGUINAL HERNIA The cadaver was that of a white male forty-nine years old. The lipoma was 30 mm. in length and 14 mm. in diameter, well-defined, lobulated and cylindrical in form and similar in color and gross structure to the fairly abundant adipose tissue present in the subperitoneal layer, with which it was directly continuous (fig. 2) . It was firm from the hardening effects of the embalming fluids and attached by its base opposite to the center of Hesselbach's triangle, while its longitudinal axis was directed caudalward and lateralward toward the angle formed by the inferior epigastric artery and the inguinal ligament. The lipoma in its descent had pierced the facia transversalis and the contiguous aponeurotic portion of the. transversalis muscle, both of which — -especially the former — were very much thinned and scarcely traceable as distinct coverings. The remainder of the overlying falx inguinalis was also distinctly thinned but had not yielded. It is to be observed that the protrusion took place at the weakest point of the falx inguinalis (conjoined tendon) or at the pars intermedia. The apex of the lipoma emerged a little below the inferior border of the falx and at that point entered the connective tissue interval between the fascia cremasterica and the process infundibuliformis of the fascia transversalis. In other words it 294 FRANK E. BLAISDELL, SR. was located in the inguinal canal between two of the coverings of the spermatic cord, a little superior and lateral to the subcutaneous ring. There was no evidence of traction upon the peritoneum, which passed normally over the site of the growth. Neither was there any evidence of an abdominal cicatrix, indicating that an operation had ever been performed upon the anterior abdominal walls. The lipoma was easily pulled from its bed, there being no adhesions and the little finger could with slight pressure be passed into the cavity which it had occupied. 1 / Fig. 2 Hesselbach's triangle viewed from behind, showing the fascia transversalis in situ, with lipoma and point of emergence. Natural size, reduced £. 1, rectus; 2, art. epigastrica inf.; 3, Hesselbach's triangle; 4, subperitoneal tissue reflected medially; 5, lipoma. DISCUSSION OF CASES A case reported by Douglas (17) corresponds very closely to the one reported above. The peritoneum was smooth, and on stripping it off a small mass of fat was attached to it, and lying just lateral to the pars tendinea of the falx inguinalis. It had projected into a deep fossa, which easily admitted the point of a finger, and passed medialward and caudalward ending at the subcutaneous ring. Annandale (9) cites a case of a fatty mass projecting through the right subcutaneous ring. It proved to be a mass of subper ANATOMICAL OBSERVATIONS ON A LIPOMA 295 itoneal fat, which had come down through the abdominal wall in the direction of a hernia, pushing before it the fascia transversalis, breaking through the fibers of the falx inguinalis, but forcing the external spermatic fascia in front of it. The peritoneum was quite smooth and free from depression. He cites another case — that of a male — in which a similar protrusion was present on each side and "both contained a peritoneal sac." From the literature it appears that the presence of a peritoneal sac is the rule, and Annandale (9) was the first to draw attention to the practical importance of recognizing and carefully examining these fat masses during operations for the relief of hernia. For a fuller account of cases and the anatomical conditions, the reader should consult Hutchinson's (15) and Wernher's (10) papers. De Garmo (25) in his work on Abdominal Hernia, states that "Elongated pieces of fat occupying the canal (inguinal) and protruding at the external ring, with or without hernia, are extremely common." Most all the text-books on pathology and surgical pathology mention their frequency and the part they play in opening up the way for a future intestinal or omental protrusion. Hence although a lipoma may be small, it may nevertheless be a potential factor in bringing about conditions which could lead tc error in diagnosis. CONCLUSIONS Douglas from his study of lipomata simulating direct inguinal herniae, surmised that the development in some cases is as follows: 1. "The formation of a hollow in the wall, the transversalis tendon in its weakest part yielding under the pressure of a mass of fat." 2. "The filling of this fossa by a peritoneal pouch." 3. "The entrance of intestine or other contents into the sac thus formed." In the case reported there was no evidence of a hollow, for the tranversalis tendon was in its usual plane throughout. The protrusion was abruptly through the fascia transversalis and the 296 FRANK E. BLAISDELL, SR. only part of the transversalis tendon affected was that immediately over the protruded fat. From the study of the case I concluded that the giving way of the parts was sudden and that the contiguous subperitoneal tissue was immediately engaged in the break, for when the lipoma was examined, it could partly be spread out in continuity with the subperitoneal tissue and contained three small lobules of fat. The possibility of the protrusion ever having given any trouble was in all probability more or less remote. It appears that in this instance the cause of the lipomatous formation was a small rupture of the fascia transversalis and the contiguous deep lamina of the falx inguinalis, through severe straining as during the act of heavy lifting, during defecation or through a blow upon a tense abdomen. Although it is not improbable that the protrusion may have formed gradually in the development of the tumor. The anatomical structure of the falx inguinalis in this case was not carefully studied. The series of four cadavers and others that were carefully studied showed that the falx is subject to marked variation, in the relative thickness of the aponeuroses of the internal oblique and trasversalis muscles not only in different individuals, but in the same individual. The aponeurosis of the transversalis is the chief factor in forming Hesselbach's ligament. The two aponeuroses vary in the degree to which they unite to form the falx inguinalis. In one of the cadavers examined the aponeurosis of the internal oblique and transversalis were quite separate down to the os pubis. The internal oblique plaj^ed but little part in the formation of the falx, and was distinctly muscular over the triangle, while the aponeurosis of the transversalis was broadly composed of white fibrous tissue and exhibited the differentiation into the three parts already described. ANATOMICAL OBSERVATIONS ON A LIPOMA 297 LITERATURE CITED (1) Morgani 1745 Cited from Douglas, Edin. Med. Jour., vol. 35, ii, 1889-90. (2) Pelletan 1810 Cited from Douglas, Edin. Med. Jour., vol. 35, ii, 1889 90. (3) Scarpa, Antoine 1823 Traitc pratique des hernies. Traduit de L'ltal ien per M. Cayol, Paris. (4) Cooper, Sir Astley P. 1804 and 1827 The anatomy and surgical treat ment of inguinal and congenital hernia. London, 1804; also 2 pts., 2 ed. by Aston Key, X, 79 pp. 17 pi., ii. 1. fol., London. (5) Cloquet, M. Jules 1835 Anatomical description of the parts concerned in inguinal and femoral hernia. London, Translated from the French by A. M. McWhinnie. (6) Maunder, C. F, 1864 Lipoma in the inguinal region, simulating hernia. London Hosp. Reports, vol. i, p. 121. (7) Paget, J. 1865 Lectures on surgical pathology, pp. 396^02. (8) Gascoyen, Geo. G. 1865-66 Fatty tumors in the scrotum. Pathol. Socs. Trans., vol. 17, p. 176. (9) Annandale, Thomas 1870 On fatty hernia. Edin. Med. Jour., ii, Jan uary, June, p. 769. 1868 Notes on tumours. Brit. Med. Jour., vol. 1, p. 162. (10) Wernher, 1869 Von Den Fettbriichen und den bruchahnlichen Fettge schwiilsten. Virchows Archives, Bd. 47, p. 178. (11) Gay, John 1872 Case of Enteritic obstruction with a rare form of fem oral hernia. Pathol. Trans., London, p. 95. (12) Butlin, H. T. 1874-75 Fatty tumour removed from the inguinal canal during the operation for hernia. Pathol. Socs. Trans., vol. 26, p. 186. (13) Tillaux, P. 1879 Traite D'Anatomie Topographique avec applications a la Chirurgie. Paris, vol. 2. pp. 619-663. (14) Stonham, C. 1886 Lipoma of the spermatic cord (Note). Trans. Pathol. Soc, London, vol. 37. pp. 341-458. (15) Hutchinson, Jonathan, Jr. 1886 Lipomata in hernial regions. Trans. Pathol. Soc, London, vol. 37, pp. 451-458. (16) Broca, A. 1888 Etudes sur les lipomes inguineaux et les hernies inguin ales. Paris. (17) Douglas, Kenneth M. 1889-90 Fat herniae in the inguinal region. Edin. Med. Jour., vol. 35, ii, pp. 918-921 ; also Tr. Med. Chir. Soc. Edin., NS ix, pp. 83-89. (18) Imbert, Leon 1897 Un cas de lipocele inguinal. Bull. Soc. Anat. de Paris, T. 72. (19) Shattock, S. G. 1908-09 On normal tumor-like formations of fat in man and the lower animals. Proc. Roy. Soc. Med., London, ii, Pathol. Section, pp. 207-270. (20) Barker, L. F. 1907 Anatomical terminology. (21) Piersol, G. A. 1907 Human anatomy. (22) Gray, Henry 1908 Anatomy, descriptive and surgical; 17th edition. (23) Morris, Henry, and McMurrich, J. P. 1907 Human anatomy; 4th edi tion. 298 FRANK E. BLAISDELL, SR. (24) Cunningham, D. J. 1906 Text-book of anatomy; 2d. edition. (25) De Garmo, W. B. 1907 Abdominal hernia. (26) Lawrence, Wm. 1843 A treatise on ruptures; 2d edition, XIII, 484 pp., 2 pi., 1810. The same from the 5th edition. London Ed. XVI, pp. 18-480. (27) Quain, R. 1855 Some unusual circumstances met with in operations for the relief of strangulated hernia. Med. Times and Gazette. January 6, p. 4. (28) Spalteholz, Werner 1901 Handatlas der Anatomie des Menschen.
THE DEVELOPMENT OF THE PULMONARY VEIN IN THE DOMESTIC CAT
ALFRED J. BROWN Anatomical Laboratory, Columbia University NINE FIGURES 1 A review of the literature concerning the pulmonary vein reveals the fact that the various investigators have been divided into two groups according to their method of dealing with the subject. On the one hand the older writers, such as Reisseisen (1), Sommering (2), Zuckerkandl (3) and J. F. Meckel (4) regarded the vein simply as part of the general vascular complex and consequently described its morphology with relation both to other portions of the pulmonary system and to the systemic circulation. The later investigators, as Schmidt (16), His (17), Born (18), Rose (19) and Fedorow (22) have studied the morphology of the vein as such, without reference to its relation to or possible connection with, the extrapulmonary vascular system. They have thus not defined the proper position of the vein in the vascular complex. The first important contributions were those of Reisseisen (1) and Sommering (2). They established the fact that the bronchial and pulmonary veins communicate freely within the lung and that the bronchial veins empty, either directly or through subordinate branches, into the azygos and hemiazygos veins and thus into the systemic circulation. J. F. Meckel (4) accepted the results of Reisseisen and Sommering, and further noted instances in which the pulmonary veins communicate through large or small radicles with the systemic circulation. He states: 1 Expense of illustrations borne by author. 299 THE ANATOMICAL RECORD, VOL. 7, NO. 8 SEPTEMBER, 1913 300 ALFRED J. BROWN Hochst merkwiirdig ist es, class nicht bloss in diesem feinen Gefassnetze (i.e. on the surface of the lung), sondern auch zwischen den grosseren Zweigen und Asten der Lungen- unci Luftrohrengef asse bedeutende Anastomosen Statt finden. Die Bronchialvenen senken sich sogar grosstentheils in die Lungen blutadern, nur die an der Wurzel der Lungen befindlichen treten zu kleinen Stammen zusammen, welche sich in die unpaarige Vene oder die obere Hohlader, oder untergeordnete A\ste des Korpervenensystems einsenken. Aus dieser Anordnung ergibt sich daher: 1. dass auch im normalen Zustande in den Lungen sehr bedeutende Communicationen zwischen dem Systeme des rothen und clem des schwarzen Blutes Statt finden; 2. dass die als Abweichungen bisweilen erscheinenden, wo grossere Gefasse der entgegensetzten Systeme sich auf dieselbe Weise verhalten, z. B. die Kranzblutadern des Herzens sich in die linke Vorkammer, eine oder mehrere Lungenvenen in die Hohlvene einsenken, eine grosse uberzahlige Lungenpulsader von der abstiegenden Aorta entsprang u.s.w., nur weitere Entwicklungen dieses Typus sind, und 3. die wichtige Bemerkung, class cliese Anastomosen in den Fallen, wo die Lungenpulsader verschlossen oder betrachtlich verengt war, und dennoch das Leben bedeutend hoch gebracht wurde, hochst warhscheinlich die Wege sind, clurch deren Erweiterung das Blut in die Lungenpulsadern geftihrt wurde. In der That werclen auch unter dieser Bedingung die Luftrohrenaste erweitert gefunden. Many other authors, among them Hyrtl (5), Gegenbauer (6), Krause (7), Winslow (8), Bohmer (9), M. J. Weber (10), Arnold (11), and W. Gruber (12) note connections between the veins of the pulmonary and systemic circulations and describe them as anomalies or variations. Zuckerkandl (3) was the first to undertake the study of these problems. In a careful and masterly paper he both added to our knowledge of the pulmono-systemic anastomoses and attempted to account for and interpret the origin of the system as a whole by reasoning from his findings in the infant and adult. His work was carried out for the most part on the bodies of children which had been injected through the pulmonary vein with a thin colored injection mass. He found that the mass fills not only the pulmonary veins, but also the bronchial veins and through them the azygos, hemiazygos and mediastinal network of veins and in many cases reaches even the postcava and the gastric veins. The anastomoses between the pulmonary and sys PULMONARY VEIN IN THE DOMESTIC CAT 301 temic veins vary in size in different individuals, and within small limits vary in position, but the pulmonary veins regularly anastomose with the veins of the mediastinal network. He concludes, therefore, that the anomalies cited are caused by a local overgrowth of a capillary plexus in one position with a corresponding underdevelopment at the point where the vein in question should normally develop. In this manner he reasons that probably the pulmonary and systemic veins are merely remnants of an originally great indifferent plexus of capillaries from which lines of drainage have been developed as best suited to the functions of the part. Subsequent to the work of Zuckerkandl attention appears to have been confined mainly to the consideration of the pulmonaiy vein itself, and especially to the relation of its opening into the heart in the various stages of its development. Boas (13), Goette (14), and Hochstetter (15) describe the opening of the pulmonary vein into the auricle in the dipnoean, amphibian and reptile. Boas divides the sinus venosus into two portions. The left, which is the smaller receives the opening of the pulmonary vein. How it subsequently reaches its final position in the left auricle he does not definitely demonstrate. Goette considers that the vein first grows out from the sinus venosus, is then cut off from this and finally establishes its definitive orifice in the left auricle. Hochstetter merely states that the pulmonary vein opens first into the sinus venosus and subsequently in the left auricle. Schmidt (16) studies the opening of the pulmonary vein in the pig embryo. In the embryo of 7 mm. he describes the vein as passing ventrally through the dorsal mesocardium to empty into the left portion of the sinus venosus, which is situated to the left of the common opening of the pre- and postcardinal veins. He then describes the absorption of the proximal segment of the vein into the auricular wall with the subsequent inclusion of its tributaries until four separate pulmonary veins empty into the auricle. The description of the opening of the vein in the left portion of the sinus venosus in the pig at this stage agrees with 302 ALFRED J. BROWN the conditions found in the cat embryo of a slightly earlier stage, that is, 5 to 6 mm. His (17) demonstrates the pulmonary vein as opening into the left portion of the sinus venosus in an early stage in the human embryo. The opening is situated to the left of the left valve of the sinus. The shift of position of the opening to its definitive site is the result of the progression of this valve to the left to join the lower portion of the septum superius on the posterior wall of the auricle. Born (18), Rose (19), and Narath (20) describe the vein as opening into the auricle but do not consider the early stages in detail. Flint (20) devotes the major part of his attention to the pulmonary arteries and bronchi and mentions the pulmonary vein only in passing. In the 5 mm. pig embryo he notes the presence of a plexus around the esophagus and describes the pulmonaiy vein as growing out from the sinus venosus. He states that from the sinus it passes dorsad in the dorsal mesocardium to the pulmonary anlage which at this stage is only partially separated from the esophagus. The venous radicles anastomose with the capillary plexus around the esophagus and pulmonary anlage thus forming a direct line of communication which leads from the ventral aspect of the pulmonary anlage to the dorsal wall of the sinus venosus. He makes no attempt to define the limitations of the plexus which he notes around the esophagus and consequently fails to recognize that it is only a part of a rich plexus which is present throughout the entire length of the gut and communicates freely with the adjacent systemic veins thus serving as a groundwork for future drainage lines between the respiratory and systemic circulations. His statement that the pulmonary vein grows out from the sinus venosus is not substantiated by any detailed evidence, nor does he explain the method by which this vein joins with the plexus around the pulmonary anlage. Fedorow (22) describes the development of the pulmonary vein in the amphibian, reptile, bird and mammal and concludes that the vein is an outgrowth of the dorsal wall of the sinus veno PULMONARY VEIN IN THE DOMESTIC CAT 303 sus at a point situated to the left of and above the opening of the cornua of the sinus. This opinion he bases on the fact that in the posterior wall of the sinus, not far from the auricle, he observed a proliferation of endothelium which projects into the dorsal mesocardium. Into this the cavity of the sinus tunnels and forms a single trunk which, a short distance from the sinus, gives off branches. These at a later stage, join with the capillaries of the pulmonary anlage and thus complete the pulmonary vein. The subsequent behavior of the venous opening he describes as follows: 1. Der Teil des Sinus venosus, in den die Lungenvene einmundet, wird infolge des ungleichen Wachstums verschiedener Abschnitte der Herzwand in die Vorkammerwand mit aufgenommen. Auf diese Weise fliesst jetzt die Vene in den gemeinsamen Teil der Vorkammer ein, d.h. mehr kranial als sie friiher einmiindete. 2. Die weite Sinusmiindung verengt sich, indem eine besondere Falte der Herzwand an der Grenze zwischen dem Sinus und der linken Vorkammer von links nach rechts riickend nach innen einwachst ; diese Falte nenne ich den "Vorkammerboden." Die Venenmiindung bleibt dabei kranial vom Vorkammerboden liegen. 3. Indem die Vorkammerscheidewand allmahlich hoher wird und mit ihrer Insertion einenimmergrosseren Teil der Vorkammerwand einnimmt, erreicht sie die Venenmiindung und lasst friiher oder spater dieselbe links von sich liegen; claim wachst die Seheidewand mit dem Vorkammerboden zusammen und die Venenmiindung wird jetzt der linken Vorkammer gehoren. The above description of the course of the orifice of the vein as it passes to its definitive position in the left auricle immediately raises the question whether the 'Vorkammerboden' which he describes is other than the left valve of the sinus venosus. If it is the left valve of the sinus his description of its shift to the left to fuse with the lower portion of the septum superius corresponds with that of His. v. Mollendorf (23) disagrees with the findings of Goette and Fedorow as to the sprouting of the pulmonary vein from the sinus venosus. He considers that the vein is connected from the first with the capillary plexus around the pulmonary anlage and with the sinus venosus. He does not concern himself with the formation of the final opening of the vein into the left auricle, nor does 304 ALFRED J. BROWN he recognize the connection of the capillaries around the pulmonary anlage with those of the surrounding systemic vascular system. He further differs from all other observers in that he states that from the first there are two pulmonary veins which empty into the sinus venosus by separate orifices. From the foregoing review of the literature it will be seen that our knowledge of the morphology of the pulmonary vein is incomplete in two main points, namely, (1) The anlage of the vein and its connection with the sinus venosus has not been described in detail ; and (2) the method by which the vein changes its orifice in the center of the sinus venosus for one in that portion of the sinus which lies to the left of the left sinus valve has not been considered. In addition, the general relation which the pulmonary venous system bears to the systemic has been entirely neglected in the study of the embryology of the vein. It is the purpose of the present paper to follow the development of the pulmonary vein of the domestic cat from the early stage in which it empties into the cephalic portion of the sinus venosus in the median line to the stage in which it attains its definitive connection with the left auricle. At the same time, its relation to the systemic circulation will be considered from the standpoint of the drainage lines which exist normally in the infant and adult as shown by Zuckerkandl, enlargement of which gives rise to the so-called anomalies. The material used in this investigation consisted of embryos of the domestic cat in the embryological collection of the Department of Anatomy of Columbia University. These were imbedded in paraffin, for the most part sectioned at 13.32^ and stained with hematoxylin (Delafield) and Orange G after the method of Morris (24). A few of the smaller embryos were stained in toto with borax carmine before being imbedded and sectioned. The embryos studied ranged in size from 4.5 mm. to 7 mm. When deemed necessary reconstructions were made by the method of Born. The complete list of embryos studied is as follows : Nos. 82, 93, 134, 469, 4.5 mm. in length. No. 226, 5 mm. in length. PULMONARY VEIN IN THE DOMESTIC CAT 305 Nos. 103, 110, 5.5 mm. in length. Nos. 84, 85, 109, 115, 116, 117, 128, 187, 283, 481, 482, 6 mm. in length. Nos. 129, 130, 131, 186, 261, 6.5 mm. in length. Nos. 105, 108, 119, 121, 135, 137, 138, 266, 281, 487, 488, 7 mm. in length. In addition, the process of development as outlined below has been substantiated by observation made upon the embryos of the chick in the Columbia collection, and the presence of the plexus around the esophagus and pulmonary anlage and its connection with the surrounding systemic veins has been observed by A. M. Miller 2 in connection with the developing blood cells in the mesenchyme of the chick. The development of the vein, so far as it will be considered in this paper, may be divided conveniently into three stages according to the point of entrance of the vein into the venous portion of the heart, namely, (1) a stage in which the vein empties into the cephalic portion of the sinus venosus in the median line, (2) in which it empties into the sinus venosus to the left of the left sinus valve, and (3) in which it empties into the left auricle. 1, First stage: embryos of 1^.5 mm. (figs. 1 and 2) The heart consists of a single tube so twisted upon itself that the ventricular portion lies ventrad and caudad and the auricular portion dorsad and cephalad. At the dorso-cephalic extremity of the auricle the ducts of Cuvier unite to form the sinus venosus. Dorsal to and at a level slightly cephalad of the sinus venosus, the tracheal furrow on the ventral aspect of the gut ends in a slight dilatation, the pulmonary anlage. In the mesenchyme surrounding the intestinal tract throughout its entire length are many capillaries. For the most part these have formed a netlike plexus which anastomoses freely with the adjacent veins of the systemic circulation. In some places the plexus is incomplete and is represented by unconnected venous spaces, the anlages of capillaries. The anastomoses with the surrounding veins may be divided into Personal communication. 300 ALFRED J. BROWN cephalic and caudal groups; the cephalic group communicates with the capillaries around the aorta and with the precardinal and segmental veins and the caudal with the omphalo-mesenteric and postcardinal veins. The irregular network already shows a tendency to the formation of longitudinal drainage lines along the lateral and dorsal aspects of the intestine. The plexus will be designated the 'splanchnic plexus' (fig. 1, 10). In addition to the communications with the systemic veins noted above, the splanchnic plexus exhibits two well defined connections with the venous portion of the heart, (1) the cephalic or pulmonary, and (2) the caudal or postcaval. These are constant both in occurrence and position. 1. The pulmonary tap. In the region of the tracheal furrow the plexus is pushed forward by the projection of the furrow from the remainder of the intestinal tube. At its caudal extremity the plexus is very abundant, forms a network surrounding the pulmonary anlage and on the sides of the anlage the capillaries show a tendency to coalesce to form a longitudinal vein. At the ventral pole of the lung bud a common stem formed by the fusion of the capillaries of the two sides passes ventrad and slightly caudad through the dorsal mesocardium to open by a rounded orifice into the cephalic aspect of the sinus venosus in the median line, at a level cephalad of and between the ducts of Cuvier. 2. The postcaval tap. This is found caudal to the pulmonary anlage at the level at which the sinusoids of the liver are forming. It (figs. 1 and 2, 13) is formed by the junction of radicles of the lateral longitudinal lines of the splanchnic plexus which join in the median line at the cephalic limit of the liver, fuse into a single vessel which passes cephalad through the dorsal mesocardium and enters the caudal portion of the sinus venosus in the median line between the omphalo-mesenteric veins at a point opposite the opening of the vein from the pulmonary anlage. The caudal and cephalic taps are connected along the sides of the esophagus by the lateral longitudinal drainage lines before-mentioned. At this stage the pulmonary vein exists as a single vessel having two main vascular connections, namely, (1) ventrally a single rounded orifice in the sinus venosus, and (2), dorsally a connec PULMONARY VEIN IN THE DOMESTIC CAT 307 fcion with that portion of the splanchnic plexus which is pushed forward by the growing pulmonary anlage, which it joins at the ventral pole of the lung bud. If the possible routes of blood flow from the pulmonary anlage be considered it will readily be seen that aside from the main channel through which the blood is returned to the heart, there exist many subsidiary paths by which the blood may reach the systemic circulation. The connections with the pre- and postcardinal veins are the most important of these as they map out the future channels to the hemiazygos and azygos veins and thus in the adult form the bronchial veins. This rich plexiform network of the splanchnic plexus with its abundant inosculation with surrounding vessels explains the various anomalies of the pulmonary veins heretofore described, and explains also the normal communications which, as pointed out by Zuckerkandl, exist between the pulmonary, systemic and portal systems. In fact, the presence of this plexus with its communications with the heart through the pulmonary vein and with the systemic and portal systems through its connection with surrounding mediastinal veins fulfils the requirements of Zuckerkandl, who states: Dieser Anastomosencomplex der Lungenvenen wiirde sich leicht erklaren, wenn bekannt ware, welcher Art das Gefass-system der primaren Anlage ist und wie .sich aus demselben das respiratorisehe Netz entwickelt. Leider ist die Entwicklungsgeschichte noch nicht im Stande, hierauf eine geniigende Ant wort zu geben XJber das Verhalten der Blutgefasse zur primaren Anlage der Lunge, so wie auch uber die Entwicklung der Lungenvenen, desgleichen daruber, wie sich diese verschiedenen Gefassbezirke einers'eits zu einander stellen und andererseits ob und in welcher Weise die theilweise Ruckbildung der primaren Gefassen erfolgt, liegen keine bestimmten Untersuchungen vor. Bei genauerer Kenntniss der Entwicklungsgeschichte wird sich wahrscheinlich ergeben, dass die Verbindungen der Lungengefasse mit den bronchialen und mediastinalen, insbesondere aber die der letzteren bloss Reste von reichlichen Anastomosen sind, die vorher zwischen Lungen- und Korpervenen bestanden haben. Wenn dem so ist, wenn die Verbindungen Rest von reichlichen Anastomosen sind, so ist die Variabilitat in Bezug auf Localitat und Starke der Anastomosen leicht erklart. 308 ALFRED J. BROWN Second stage: embryos of 5 to 6 mm. (figs. 3 and 4) The most important change from the preceding stage is noted in the shift in position of the sinus venosus in its relation to the auricle. The sinus has moved caudad and to the right and now empties into the caudal and right portion of the still undivided auricle. The right duct of Cuvier (fig. 4, 7) is very short and extends dorso-ventrally to empty into the right cornu of the sinus which is situated furthest to the right. The left duct of Cuvier (fig. 4, 8) formed by the junction of the left pre- and postcardinal veins, curves caudally and to the right to empty into the left cornu which then passes horizontally to the right and joins the caudal and left portion of the right cornu. The two cornua then open into the sinus by a common orifice (fig. 4, 9). The right limit of the sinus is well defined by a reduplication of the myocardium which projects ventrad and mesad into the cavity of the auricle as a vertical fold having a ventral free margin. This fold forms the right sinus valve. It is triangular in shape with the apex of the triangle directed upward and forward and continuous on the roof of the auricle with the septum spurium. The dorsal and caudal edges are continuous with the dorsal and caudal walls of the auricle. The left limit of the sinus venosus is hard to define as it shades gradually into the wall of the auricle. The left margin of the common opening of the cornua presents a very slight reduplication of the myocardium ventrad, the anlage of the left sinus valve. On the roof of the auricle in the median line the septum superius projects downward presenting a free edge below. The dorsal limit of this septum blends with the dorsal wall of the auricle at a point to the left of and cephalad to the upper limit of the left valve of the sinus. Between the left valve of the sinus and the septum superius at a level caudal to the dorsal limit of the latter is the opening of the cephalic tap of the splanchnic plexus, the pulmonary vein. This is situated just to the right of the median line (fig. 4, 11). The caudal tap of the splanchnic plexus enters the caudal aspect of the right cornu of the sinus on the left side just previous to its junction with the left cornu. PULMONARY VEIN IN THE DOMESTIC CAT 309 The pulmonary anlage (fig. 3, 2a) is represented by a retort shaped prolongation arising from the ventral aspect of the gut at the level of the upper limit of the auricle . This extends caudad and slightly ventrad to the level of the sinus venosus. Along either side of this tube is a plexus of capillaries which at the ventral pole of the anlage forms a definite vein which passes ventrad through the dorsal mesocardium. Just dorsalto the sinus venosus (fig. 3, 11), the two veins join to form a common trunk which after a short ventrad course meets the dorsal wall of the sinus venosus and passes through it as a long funnel shaped tap to empty by the orifice described above. Cephalad the pulmonary plexus communicates with the lateral longitudinal line of the splanchnic plexus on either side. The caudal tap (fig. 3, 12) has become a well marked vein which passes cephalad just to the right of the median line to the level of the lower limit of the sinus venosus. At this point it bends sharply to the right and passes through the dorsal mesocardium behind the dorsal wall of the sinus venosus to empt}^ into the left caudal aspect of the right cornu of the sinus as described above. The connection of this vein dorsally with the left longitudinal line of the splanchnic plexus is represented only by a capillary plexus which communicates freely with the sinusoids of the liver Above the level of the upper surface of the liver, between it and the pulmonary plexus the lateral lines of the splanchnic plexus form a plexus surrounding the esophagus which communicates above with the pulmonary plexus and below with the sinusoids of the liver and through these with the postcaval tap. On the right side the caudal tap of the plexus is well formed below the level of its orifice into the sinus venosus and can now be recognized as the anlage of the hepatic and suprahepatic portions of the postcava. From the above it is clear that the change in relation of the orifices of the veins opening into the sinus venosus is the result of unequal growth in the various portions of the sinus. The opening of the pulmonary vein has followed the caudal progression of the sinus and as the growth of the two sides has been equal at this level the orifice retains its original median position in the 310 ALFKED J. BROWN sinus. Caudal to this level growth has been markedly unequal on the two sides, the left increasing in width much more rapidly than the right. As a result, the lower portion of the sinus has shifted to the right side and now opens into the caudal and right aspect of the auricle. The evidence going to prove this inequality of growth is two-fold, (1) The left duct of Cuvier and the left cornu of the sinus are long drawn out and pursue a lateral course from above downward and from left to right, while the right duct of Cuvier and the right cornu are short and pursue a dorso- ventral direction; (2) The caudal tap of the splanchnic plexus ascends in the dorsal mesocardium to the level of the lower limit of the sinus venosus, then bends sharply to the right and pursues a horizontal course behind the sinus until it reaches its entrance into the right cornu just before the fusion of the latter with the left to form a common orifice. Referring to the previous stage, the relative position of the orifice into the sinus has changed but little, the point of entrance still representing the original median line of the sinus which has disappeared through the fusion of the two cornua. The horizontal course through the dorsal mesocardium behind the sinus represents the amount of growth of the left portion of the auricular wall over that of the right . The plexus around the pulmonary anlage still retains its lines of venous drainage, the pulmonary vein draining into the systemic circulation by means of the connections of the pulmonary plexus with the cephalic portions of the lateral longitudinal lines. Below the pulmonary plexus communicates with the caudal tap by means of the esophageal plexus which represents the lateral and posterior longitudinal lines of the splanchnic plexus. In addition to these communications the well known broncho-pulmonary anastomoses in the lung bud itself are easily recognized. Third stage: Embryos of 6.5 to 7 mm. (figs. 5 and 6) The sinus venosus with the exception of the openings of the cornua has been incorporated into the auricle. The right valve of the sinus (fig. 6, 40) is very prominent and above is continued PULMONARY VEIN IN THE DOMESTIC CAT 311 into the septum spurmm which has shifted to the left and fused with the septum superius. The left valve of the sinus has likewise shifted to the left and its cephalic extremity on the dorsal wall of the auricle has fused with the dorso-caudal portion of the septum superius. As a result of the latter shift the orifice of the pulmonary vein has preceded the left valve of the sinus, passed under the septum superius, and now empties into the left auricle having both septum superius and left Valve of the sinus, or in other words, the interauricular septum on its right (fig. 6, 11). The pulmonary anlage shows a division into two lateral tubular prolongations, the anlages of the bronchi, which are surrounded by a rich capillary plexus. From the ventro-caudal aspect of each of these plexuses a well marked channel passes caudo-ventrally to unite with its fellow of the opposite side, and, after a very short course in the dorsal mesocardium, enters the wall of the left auricle, passes through it by a long funnel shaped tap and empties into the auricle by the orifice described above. From the dorso- cephalic portion of the pulmonary plexus of either side small vessels extend cephalad and dorsad to empty into the lateral longitudinal lines of the splanchnic plexus, thus mapping out the course of the future bronchial veins to the azygos and hemiazygos veins. The caudal tap of the splanchnic plexus is now a well marked vein which lies on the right side of the median line, receives the hepatic sinusoids and is plainly recognizable as the pars hepatica and suprahepatica of the postcava. The paths of communication between the pulmonary plexus above and caudal tap of the plexus below remain as many small anastomoses between the pulmonary capillaries above with the adjacent systemic veins and the communications of the latter with the postcaval tap below the septum transversum. The broncho-pulmonary anastomoses in the lung bud itself are still present. The orifice of the pulmonary vein has now, by the fusion of the left sinus valve with the septum superius, been transferred to the left auricle. The two subsidiary lines of drainage described in the previous stages are retained, but in markedly different degrees. That from the pulmonaiy plexus to the cephalic portion 312 ALFRED J. BROWN of the lateral longitudinal lines consists of several well marked channels which map out the future course of the bronchial veins. The caudal line of drainage to the postcava exists now only as small capillary anastomoses between pulmonary plexus on the one hand and the esophageal and aortic plexuses on the other, thus accounting for the irregularity of the connections between pulmonary and mediastinal veins and through the latter with the portal and postcaval systems described by Zuckerkandl. Summary. It is thus seen that the common pulmonary vein develops from the cephalic communication between the splanchnic plexus and the sinus venosus. The plexus is pushed forward by the developing lung bud and is carried ventrad and caudad as the pulmonary anlage develops. With the displacement of the sinus venosus caudad and to the right due to the inequality of growth of the two halves of the sinus and auricle, the pulmonary orifice moves only slightly to the right and empties into the left portion of the sinus, to the left of the left sinus valve and at a level below the septum superius. The formation of the interauricular septum by fusion of the left sinus valve with the dorsocaudal extremity of the septum superius definitely assigns the pulmonary vein to the left auricle. The plexus around the lung bud is differentiated into two systems, (1) from its ventral and caudal portion, the pulmonary for the fulfillment of the respiratory function, and (2) from the caudal and cephalic portion the bronchial for the venous drainage of the lung tissue proper. This is diametrically opposed to the opinion of Fedorow who states that he cannot accept the view of an originally indifferent plexus of capillaries which may develop on the one hand into veins and on the other inosculate with arteries, but believes that the vein grows directly from the dorsal wall of the sinus venosus as a bud finally to inosculate, after dividing into countless branches, with the plexus around the pulmonary anlage. while the artery approaches the opposite extremity of the plexus growing in a similar manner from the sixth aortic arch. That portion of the splanchnic plexus lying between the pulmonary anlage cephalad and the hepatic sinusoids caudad serves PULMONARY VEIN IN THE DOMESTIC CAT 313 as a temporary direct communication between the pulmonary vessels and the systemic circulation represented by the postcaval tap of the splanchnic plexus. The paths by which this circulation is carried out have already been described. With the further development of the pulmonary veins this portion of the splanchnic plexus loses its connection with the pulmonary capillaries m except for the persistence of occasional small veins which pass from the pulmonary capillaries to the esophageal or aortic plexuses, thus mapping out the communication of the pulmonary veins with the postcaval and portal systems through the veins of the posterior mediastinum. This conception of the pulmonary system, namely, that it is simply a specially developed part of an indifferent plexus originally present in this region, assigns to the vein its proper position in the general vascular complex. It also serves to explain the small communications between pulmonic and systemic circulations normally present in the adult and the large channels occasionally found which are classed as anomalies of the pulmonary veins. An anomaly of the right pulmonary vein A specimen of most unusual abnormality of the right pulmonary vein which bears out the conception of the development of the pulmonary system as given above was presented to the Anatomical Department of Columbia University by Dr. Edwards A. Park. Although previously published (25) with a short and incomplete note as to the probable etiology of the anomaly, a brief description will be given here. On ventral view (fig. 7) the heart was normal save for a small teat-like process attached to the tip of the left auricular appendage. The dorsal view (fig. 8) showed complete absence of any right pulmonary vein entering the left auricle. The right lungwas very small and compressed -against the inner wall of the thorax by the heart which in turn was pushed to the left by a very large left lung. In the main interlobar fissure of the right lung was a good sized venous channel, the pulmonary vein which, beginning in the region of the hilum ran caudad to the diaphragm, 314 ALFRED J. BROWN pierced it, and on reaching its abdominal surface turned sharply to the left to enter the right aspect of the postcava in its course between liver and diaphragm (fig. 9). The vein in this instance is a persistence, on the right side, of the lateral line of communication between the cephalic and caudal taps of the splanchnic plexus (fig. 3, 14) accompanied by a loss of 'the normal communication between the plexus on the right side of the pulmonary anlage and the common stem of the pulmonary vein. The anomaly is unusual because of the entire absence of the normal entrance of the right pulmonary vein into the left auricle, the entrance of the pulmonary vein into the postcava representing merely the enlargement of a very small channel which is frequently present in the adult mammal. LITERATURE CITED (1) Reisseisex, F. D. 1S0S Uber den Bau der Lungen. Berlin, 1S0S u. 1822. (2) Soemmering, Th. 1808 Uber die Struktur, die Verrichtung und den Ge brauch der Lungen. Berlin. (3) Zuckerkaxdl, E. 18S1 Uber die Anastomosen der Venae pulmonales mit den Bronchialvenen und mit dem mediastinalen Venennetze. Sitzimgsberichte der kaiserlichen Akad. der Wissenschaften. 84 Band. I Heft. Dritte Abtheilung. Juni. (4) Meckel, J. F. 1820 Handb. d. mensch. Anat., Bd. 4, Halle u. Berlin. (5) Hyrtl, J. 1880 Anatomische Variataten. Hannover. (6) Gegenbauer, C. 1880 Morph. Jahrb., Bd. 6. Leipzig. (7) Krause, W. 1876 Variataten der Korpervenen in Henle's Handb. der Gefasslehre. Braunschweig. (8) Winslow, J. B. 1868 Cited in J. Arnold's essay: Ein Fall von Cor Tril oculare, etc. Virch. Arch. Berlin. (9) Bohmer. P. A. 1770 Hist, de l'Anat. et de la Chirug. Tom. 5, Paris. (10) Weber, M.J. 1829 Uber die Varietaten der Venen. Meckel's Arch. Leip zig. (11) Arnold, F. 1850 Handb. d. Anat. des Menschen. Bd. 2, Freiburg imBreis gau. (12) Grtjber, W. 1870 Ein Fall von'Einmundung der Vena pulmonalis dextra superior in die Cava superior. Virchow's Arch.. Bd. 68, Berlin. (13) Boas, J. E. V. 1880 Uber Herz und Arterienbogen bei Ceratodus und Pro topterus. Morph. Jahrb., Bd. 6. 1883 Beitrage zur Angeiologie der Ainphibien. Morph. Jahrb. Bd. 8. PULMONARY VEIN IN THE DOMESTIC CAT 315 (14) Goette, A. 1875 Die Entwickelungsgeschichte der Unke (Bombinator ig neus) als Grundlage einer vergleichenden Morphologie der Wirbeltiere. Leipzig. (15) Hochstetter, F. 1903 Die Entwickelung des Blutgefasssystems. Hert wig's Handb. der Entwickelungslehre der Wirbeltiere. Bd. 3, T. 2, 4 Kap. L908 Beitrage zur Entwickelungsgeschichte der europaischen Sumpf schildkrote (Emys lutaria marsili). 2. Die ersten Entwickelungs stadien der Lungen and die Bildung der sogenannten Xebengekrose. Denkschr. d. kais. Akad. d. Wiss. Wien 84. (16) Schmidt, F. T. 1870 Bidtrag til Kundskaben orn Hjerteb Undviklungshis torie. Nordiskt medic. Arkiv. Vol. 2. Xr. 23. 1870. Deutsches Referat von P. L. Panum im Jahresberichte iiber die Leistungen und Fortschritte in der gesammten Medizin von Virchow und Hirsch, 5, Bd. 1. (17) His, W. 1885 Anatomie menschlicher Embryonen. T. 3, Leipzig. 1887 Zur Bildungsgeschichte der Lungen beim menschlichen Embryo. Arch. f. Anat. u. Phys. Abt. f. Anat. (18) Born, G. 1SS9 Beitrage zur Entwickelungsgeschichte des Saugetierher zens. Arch, fur mikr. Anat., Bd. 33. (19) Rose, C. 1888 Beitrage zur Entwickelungsgeschichte des Herzens. Inaug. Dissert. Heidelberg. 1889 Zur Entwickelungsgeschichte des Saugetierherzens. Morph. Jahrb., Bd. 15. 1890 Beitrage zur vergleichenden Anat. des Herzens der Wirbeltiere. Morph. Jahrb., Bd. 16. (20) Xarath, A. 1901 Der Bronchialbaum der Saugetiere und des Menschen. Bibliotheca medica. Abt. A. H. 3. (21) Flint, J. M. 1907 The development of the lungs. Amer. Jour. Anat., vol. 6, no. 1. (22) Fedorow, V. 1910 tjber die Entwickelung der Lungenvene. Anat. Hefte. 1 Abt. 122 Heft (40 Bd., H. 3.). (23) v. Mollendorf, W. 1912 tjber Anlage und Ausbildung des Kiemenlung enkreislaufs bei Anuren (Bombinator pachypus). Anat. Hefte, Heft 141 (47 Band). (24) Morris, J. T. 1909 A note on orange G counter-staining suggesting a useful method in the management of embryonic tissue. Anat. Rec. vol. 3, no. 12, December. (25) Park, E. A. 1912 Proceedings of the Xew York Pathological Society, New Series, vol. 12, nos. 3 and 4, p. 88, March and April. THE ANATOMICAL RECORD, VOL. 7, NO. 8 PLATE 1» Explanation of Figure 1 Schema of the left side of a wax reconstruction of a 4.5 mm. cat embryo. Columbia collection no. 134, X 200. The left cornu of the sinus venosus together with the structures entering it, has been removed. 2, gut 2a, pulmonary anlage 4, left postcardinal vein 6, left precardinal vein 8, left duct of Cuvier 9, sinus venosus 10, splanchnic plexus 11, cephalic tap of the splanchnic plexus into the cephalo-mesial portion of the sinus venosus (common pulmonary vein) 12, communications between splanchnic plexus and precardinal vein caudal tap of splanchnic plexus (hepatic portion of postcava) communications between the splanchnic plexus and postcardinal vein 13 U The engravings in this paper were supplied by the author. 316 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 1 KfL — HimLSi 317 I- LATE 2 ExPLAXATIOX OF FlGURE 2 Composite drawing of super bryo, Columbia collection no. 134, reduced; schematic. 1, aorta 2, gut 2a, pulmonary anlage 3, right postcardinal vein 4, left postcardinal vein 5, right precardinal vein 6, left precardinal vein 7, right duct of Cuvier 8, left duct of Cuvier 9, sinus venosus 10, splanchnic plexus imposed cross sections of the 4.5 mm. emin the region of the cervical bend, X 150, 11, cephalic tap of splanchnic plexus 1 common pulmonary vein I 1-j. caudal tap of splanchnic plexus (hepatic portion of postcava) 15, neural tube 16, coelom 17, right umbilical vein 18, left umbilical vein 19, right omphalo-mesehteric vein 20, left omphalo-mesenteric vein 32, liver 318 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 2 319 PLATE 3 Explanation of Figure 3 Right side of a wax reconstruction of the 5.18 nun collection, no. 226, X 150, reduced. 1, aorta 2, gut 2a, pulmonary anlage 3, right postcardinal vein 5, right precardinal vein 9, sinus venosus 10, splanchnic plexus 11, pulmonary vein embryo, Columbia 12, caudal tap of splanchnic plexus (hepatic portion of postcava) 14, remnants of former communication between the thoracic and abdominal portions of the splanchnic plexus 21, conus arteriosus 22, common ventricle 320 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 3 321 PLATE 4 Explanation of Figure 4 Wax reconstruction of the 5.18 mm. embryo, Columbia collection, no. 226, X 150, reduced. Viewed from above, the top of the common auricle having been removed. 1, aorta 2, gut 2d, pulmonary anlage 4, left postcardinal vein 7, right duct of Cuvier 8, left duct of Cuvier 9, common opening of the cornua into the sinus 10, component parts of the splanchnic plexus 11, pulmonary vein 21, conus arteriosus 23, common auricle 38, auriculo-ventricular orifice 322 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 4 323 PLATE 5 Explanation of Figure 5 Wax reconstruction of the heart of the 7 mm. embryo, Columbia collection, no. 266, X 75, reduced. Viewed from behind showing the crossing of the left duct of Cuvier to the right consequent to the shift of the sinus venosus. 2a, pulmonary anlage 9, right cornu of the sinus venosus 3, right postcardinal vein 11, pulmonary vein 4, left postcardinal vein 13, caudal tap of the splanchnic plexus 5, right precardinal vein (hepatic portion of postcava) 6, left precardinal vein 22, common ventricle 7, right duct of Cuvier 26, right auricle 8, left cornu of the sinus venosus 27, left auricle 324 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 5 325 PLATE 5 Explanation of Figure 5 Wax reconstruction of the heart of the 7 mm. embryo, Columbia collection, no. 266, X 75, reduced. Viewed from behind showing the crossing of the left duct of Cuvier to the right consequent to the shift of the sinus venosus. 2a, pulmonary anlage 9, right cornu of the sinus venosus 3, right postcardinal vein 11, pulmonary vein 4, left postcardinal vein 13, caudal tap of the splanchnic plexus 5, right precardinal vein (hepatic portion of postcava) 6, left precardinal vein 22, common ventricle 7, right duct of Cuvier 26, right auricle 8, left cornu of the sinus venosus 27, left auricle 324 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 5 325 PLATE 6 EXPLANATION OF FIGURE 6 Wax reconstruction of the 7 mm. embryo, Columbia collection, no. 266, X 75, reduced. Viewed from above, the top of the auricles having been removed. 22, common ventricle 26, primitive right auricle 27, primitive left auricle 38, auriculo-ventricular orifice 39, right valve of the sinus venosus 40, anlage of the interauricular septum /, aorta 2a, pulmonary anlage 8, left cornu of the sinus venosus 9, sinus venosus 11, pulmonary vein 21, conus arteriosus 326 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 6 327 PLATE 7 Explanation of Figure 7 Ventral view of congenitally abnormal heart. 24, right ventricle 34, arch of the aorta 25, left ventricle 35, innominate artery 26, right auricle 36, left common carotid artery 27, left auricle 37, left subclavian artery 29, left pulmonary vein 46, precava 81, left pulmonary artery 8 Dorsal view of congenitally abnormal heart. 24, right ventricle 25, left ventricle 26, right auricle 27, left auricle 29, left pulmonary vein 30, right pulmonary artery 31, left pulmonary artery 33, azygos communis vein 34, arch of aorta 35, innominate artery 36, left common carotid artery 37, left subclavian artery 46, precava 47, postcava 9 Schema of abnormal pulmonary has been removed. 28, right pulmonary vein 29, left pulmonary vein 30, right pulmonary artery 31, left pulmonary artery 34, arch of aorta circulation, ventral view. The heart 41, right inferior phrenic artery 44, right lung 45, left lung 46, precava 47, postcava 328 PULMONARY VEIN IN THE DOMESTIC CAT ALFRED J. BROWN PLATE 7 36 37 Anatomists and zoologists, as well as other investigators who are adding so materially to the fundamental knowledge upon which scientific medicine is based, who depend upon the use of living animals for their researches, will be gratified to realize that one of the leading popular magazines has taken a firm stand in favor of scientific medical progress. From the August 16th issue of Harper's Weekly, now edited by Norman Hapgood, we clip the following: A.NTI-VIVISECTION Some dozens of letters have come to us all at once, asking us to be fair in the vivisection controversy and to give "both sides." Some of these letters inform us that the writers will subscribe to this Weekly if we are fair, but not if we pursue a course hostile to the anti-vivisection crusade. We have no intention of giving both sides. On the contrary, the support of the cause of scientific medical progress will be one of the things to which we shall be energetically devoted. We shall no more give both sides of the argument on experiment than we shall give both sides of the question of whether the household fly shall be encouraged in the diningroom, or sewers emptied into the city reservoir, or swamps kept for the breeding of mosquitoes, or smallpox patients permitted to ride on the street cars. We shall be extremely bigoted on the subject, and shall hope that the day will soon come when cancer will be added to the great diseases that have yielded to investigation.
Cite this page: Hill, M.A. (2024, April 25) Embryology Paper - Observations on the peripheral distribution of the nervus terminalis in mammalia (1913). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Observations_on_the_peripheral_distribution_of_the_nervus_terminalis_in_mammalia_(1913)
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