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An Afferent Hippocampal Fiber System in the Fornix of the Monkey

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An Afferent Hippocampal Fiber System in the Fornix of the Monkey An Afferent Hippocampal Fiber System in the Fornix of the Monkey CHARLES L. VOTAW AND EDWARD W. LAUER Department of Anatmy, The University of Michigan, Ann ATboT, Michigan In a previous investigation (Votaw, ’60b) and weighed from 2.2 to 5.3 kgs. Seven it was noted that, in spite of massive bilat- were used only for this investigation and eral removal of the hippocampal formation seven others were used as well in another (Ammon’s horn and dentate gyms), there investigation on the function of the hippo- was a considerable percentage of the fi- campus and are included in this study bers in the fornix, anterior to the hippo- because the lesions placed were ideally carnpal commissure, that did not degener- suited for comparison with the former ate. This would imply, since the lesions seven cases. to all intents and purposes eliminated all All animals were subjected to aseptic possible fibers going into the fornix from surgical procedures. The only surgical pro- the region of the temporal lobe, the pres- cedure on seven was the production of the ence of fibers in the fornix which are a€- lesions to be reported here; lesions were ferent with respect to the hippocampus, placed in the remaining seven after other and further, that these fibers are not com- studies had been carried out. General missural in nature. In another study anesthesia was used and consisted of (Votaw, ’60a), it was shown that lesions ether, sodium pentobarbital (20-25 mg/kg in the septa1 area would produce a de- of body weight given intravenously) or a generation which could be followed from combination of the two anesthetics, ether the area of the lesion in a caudal direction, being used to supplement a somewhat coursing through the body of the fornix, lower dose of sodium pentobarbital. Fol- from which it would enter the fimbria and lowing closure of the surgical wounds, the alveus. The final termination could not be animal was given a dose of penicillin- determined with certainty. chloramphenicol intramuscularly and re- There is accumulating in the current turned to an isolated cage. The monkeys literature a considerable body of evidence were observed daily, and additional anti- concerning a hippocampal afferent sys- biotics given if it was thought necessary. tem in the fornix (see Discussion). Some Wound infection was limited to one case, of this information is gained from morpho- and a post-operative diarrhea was evident logical experimentation, but the majority in two others. These complications were of the more suggestive evidence is based easily controlled. on physiological data. To the authors’ In four of the animals, a dorsal ap- knowledge there is no information avail- proach was used. A craniectomy was ac- able with respect to the monkey about this complished over the motor area. Then a fiber system, except that quoted above small portion of the medial cerebral cortex (Votaw, ’60a). In an attempt to investi- was removed until, with gentle retraction, gate more fully the existence of such a the corpus callosum could be visualized. fiber system in monkeys, and, if possible, A small opening was next made in the to describe some of its relations, the pres- corpus callosum exposing the easily iden- ent study was undertaken. tified bodies of the fornices. Using a spe- cially prepared hooked knife, the bodies of MATERIALS AND METHOD the fornices were lifted away from the Fourteen monkeys (Macaca mulatta) were used in these experiments. The ani- 1This work was supported by National Science Foundation Grant 6-11433 for which the authors mals were unselected with respect to sex, express their appreciation. 195 196 CHARLES L. VOTAW AND EDWARD W. LAUER thalamus, and then sectioned. In one ad- further clarification was necessary, they ditional animal, the opening was made were mounted and examined. more anteriorly, and the lesion produced Precautions were taken to eliminate the by aspirating the septal area and the artifacts which are inherent in the Marchi anterior columns of the fornix. technique. However, a small proportion of In two cases, electrodes were placed normal fibers were stained, and there was stereotaxically in the septal areas. Follow- the appearance of some “Marchi dust” ing stimulation of the septal area for an- in the sections. The only degeneration to other study, electrocoagulation was carried be described will be that which could be out at the tip of the electrode placements. followed serially from the lesion, and In each of the remaining seven animals, which had the characteristic black irregu- a craniectomy was performed over the su- lar shapes of Marchi degeneration. Termi- perior part of the temporal lobe of the nal degeneration is not revealed by this brain. After exposure of the superior and method, and, accordingly, nothing but the middle temporal gyri, an opening was most tentative suggestion will be made made through these gyri, using the su- about the exact termination of the fibers perior temporal fissure as a guide. This to be described. Primary concern in this procedurc was followed until the temporal study is with the make-up of the fornix. horn of the lateral ventricle was opened Therefore, detailed descriptions of the de- and the hippocampus could be seen as the generation in the projections of the fornix ventromedial wall of the ventricle. Elec- system which have been presented else- trodes were then placed visually and the where (Votaw, ’60b) will not be given hippocampus explored by electrical stimu- here, and reference will be made to those lation, with results which will be presented results only for comparison. in another paper. Following this proce- The term hippocampal formation (or dure, lesions were made in the hippocam- hippocampal complex), as it is used in pus using either an aspirator or a special the literature, includes the dentate gyrus, dissection instrument. This procedure was cornu Ammonis, and subiculum. At times carried out in two stages, one for each the term has been extended to include side, with an interval of from 2-11 weeks. the presubiculum and even the entorhinal In four of these seven animals, this was area. The term hippocampus is usually the only procedure. In the othcr three, used to indicate the cornu Ammonis alone the procedure just described was preceded although some earlier authors have used by a fornicotomy as outlined previously. it as synonymous with hippocampal for- Thus, in four animals there were bilateral mation. In this study, the term hippo- lesions of Ammon’s horn, and in three ani- campal formation (or hippocampal com- mals there were bilateral lesions of Am- plex or hippocampal area) will be used mon’s horn plus an additional section of to indicate the complex of dentate gyrus, the fornix bilaterally. Ammon’s horn and subiculum. The pre- After survival periods of from 21 days subiculum and entorhinal area will be to 3.5 months, the animals were killed by treated as separate entities. The terms an overdose of evipal and perfused intra- hippocampus and cornu Ammonis (Am- cardially with 10% formalin. The brains mon’s horn) will be used interchangeably were removed immediately and addition- ally fixed for a period of not less than two RESULTS weeks in 10% formalin. They were then Lesions of septal nuclei. In one case sectioned in 2 mm slices which were left there was complete removal of the medial in the fixative fluid for an additional week. and lateral septal nuclei of the left side. They were then stained according to the This lesion also interrupted the column of Marchi technique as modified by Swank the homolateral fornix and slightly in- and Davenport (’35). Sections were cut jured the column of the other side. The at 30 to 50 CI depending on the friability anterior commissure was involved and of the tissues. Every fifth section was degeneration was observed within it. In mounted and studied microscopically. The addition, there were the lesions in the intermediate sections were stored, and if corpus callosum and in the frontal lobe. HIPPOCAMPAL AFFERENT FIBERS 197 In the other two cases there were small tion should not be involved at all, have a circumscribed lesions bilaterally, but asym- large amount of such dust. Therefore, it metrically located in the medial and lat- is not known to what position in the hippo- eral septal nuclei. The electrode paths campal formation the fibers under study could be followed to the area of the lesion, go. Since there was no degeneration be- but the amount of degeneration about yond the region of the hippocampal for- them was insignificant. The anterior com- mation (subiculum, presubiculum, hippo- missure and the anterior columns of the campal gyrus), it is assumed that the fi- fornix were not involved in these lesions. bers terminated somewhere in that forma- The degeneration resulting from these tion. lesions tended to be largely ipsilateral, as In all three of these cases, but espe- can be determined from the first case. cially in the case in which the septal nuclei However, there was a significant number were entirely removed, degeneration can of degenerated fibers on the contralateral be followed in the postcommissural fornix side. Degeneration could be followed in a column to the medial mammillary nucleus posterior direction in the bodies of the for- and other hypothalamic nuclei. No post- nices. This degeneration was somewhat mammillary degeneration could be found. diffusely dispersed throughout the body Some degeneration was found as well in of the fornix but the region of heaviest the diagonal band of Broca and a very few concentration was found to be on the degenerated fibers were observed in the lateral side of the fornix. Anteriorly, where lateral region of the hypothalamus.
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