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Afferent Connexions of the Allocortex by B J. Anat. (1965), 99, 2, pp. 339-357 339 With 2 plates and 6 text-figures Printed in Great Britain Afferent connexions of the allocortex By B. G. CRAGG Department of Anatomy, University College, London INTRODUCTION The cingulate, entorhinal and retrosplenial areas are major sources of projections to the hippocampus, but little is known of any interconnexions between the neo- cortex and these allocortical areas. Adey & Meyer (1952a) described one monkey brain in which a massive temporal lesion had caused the degeneration of some fibres in the entorhinal cortex stained by the method of Glees. This result was con- firmed and refined by Whitlock & Nauta (1956) who made lesions in the inferior temporal gyrus in four monkeys, and stained degenerating fibres in the entorhinal area with the Nauta method. Another source was found by Adey & Meyer (1952b) in two monkeys with large lesions in the frontal cortex. Degenerating fibres were stained in the presubiculum by the method of Glees. After similar lesions, Showers (1958) stained degenerating fibres with the Marchi method in the cingulate and hippocampal gyri in four monkey brains. In rabbits, rats and cats, the olfactory tubercle and prepiriform cortex are sources of afferents to the entorhinal area and the presubiculum (Cragg, 1961 b). Following lesions made in the olfactory cortex, degenerating fibres were stained by the method of Nauta & Gygax (1954) in the entorhinal area and presubiculum. The dorsal and posterior part of the entorhinal area also receives a projection from the contra-lateral hemisphere by way of the dorsal hippocampal commissure (Cragg & Hamlyn, 1957). The origin of this projection is unknown. In 1951 Dr P. K. Thomas (personal communication) suggested recording the electrical potentials of the entorhinal cortex while exploring the neocortex system- atically with a stimulating electrode. One experiment, on an anaesthetized cat, was done with Dr Thomas, and a small region in the mid-suprasylvian gyrus was found to evoke electrical responses in the ipsilateral entorhinal area when stimulated electrically, or when strychnine was applied topically. A similar result was found by Niemer, Goodfellow & Speaker (1963). Small lesions have now been made in the mid-suprasylvian gyrus and degenerating fibres traced by the Nauta method to the cingulate cortex. The latter in turn has been found to give rise to some fibres that end in the entorhinal cortex, as well as to the larger projection to the presubiculum. Frontal and temporal lesions have also been made in the neocortex to test the results found in the monkey. Lesions made in several other neocortical areas did not cause the degeneration of projections to the allocortex. It appears that there are three areas of neocortex that project to the allocortex, that there are two-way inter- connexions within the areas of allocortex, and that there is an important projection from the septum to allocortex. 340 B. G. CRAGG MATERIALS AND METHODS Cats and a small number of rabbits were anaesthetized with pentobarbital sodium, and given penicillin. Brain lesions were made under sterile conditions with suction or with a coagulating current passed through an electrode. After survival periods of 7-24 days, the brains were perfused and subsequently stained by the method of Nauta & Gygax (1954) with the minor modifications set out previously (Cragg, 1961 a). The most important modification was that the fixation period in buffered neutral formol saline was not allowed to exceed 2 weeks. With this precaution satisfactory preparations were obtained from more than forty consecutive brains during the course of this study. The time of treatment with potassium perman- ganate was kept fixed at 12 min. If the intensity of staining of the first section of any batch was too weak, the ammoniacal silver bath was adjusted for the rest of the batch by adding more silver nitrate solution. Many of the fibres involved in this study were extremely fine, and did not appear in under-impregnated sections. The brains of one cat and one rabbit were fixed by immersion a few hours after death, and gave good preparations. One rabbit was perfused with Bouin's fixative for Nissl's method, and the brain was then further fixed by immersion in formol saline. This brain, too, gave satisfactory results with the Nauta method. The variability and occasional staining failures encountered with the original method are probably due to the prolonged action of the fixative rather than to the conditions at the initial fixation. In order to be able to put loose frozen sections taken at close intervals through the thalamus into strict serial order, three consecutive sections were taken at each interval (0-25 -05 mm.) and placed in a separate compartment in a plastic tray filled with formol saline solution. When the sectioning was finished, the three sections from each compartment were taken out into a large dish of water and each snicked with scissors in some particular gyrus or area irrelevant of the final analysis. The snicks were placed in different positions in the sections from the other compart- ments. One section from each compartment was then mounted in order and stained with cresyl violet after fat extraction in hot pyridine, while another section from each compartment was stained loose by the Nauta method, leaving a third series in reserve. When the Nauta sections were mounted, thev were numbered by comparing the snicks with the Nissl series. RESULT S Projections froin the sujprasylvian gyrus Lesions were made in the middle part of the suprasvlvian gcyrus in five cat brains, unilaterally in three (B1R3) and bilaterally in two (B4, 5). One brain (B 1) was cut frontally, two parasagittally (B 2, 3) and the two with bilateral lesions were cut frontally on one side and parasagittally on the other. The lesions were all similar to that in B 3 shown in Text-fig. 1, and the resulting fibrc degeneration can be described for the group as a whole. Degenerating fibres passed from the lesions through the subeallosal fasciculus to the caudate nucleus, where terminal degeneration was seen in the dorso-medial part of the head of the nucleus. A small amount of fibre degeneration was also seen in the Afferent connexiof8 of the allocortex 341 claustrum. Many degenerating fibres entered the thalamus from the dorsal part of the internal capsule and projected to no less than seven thalamic nuclei. These were the ventral parts of the nucleus lateralis dorsalis, the dorsal part of the nucleus ventralis anterior, the dorsal part of the nucleus centralis lateralis, the anterior and dorso-lateral parts of the pulvinar nucleus, the nucleus lateralis posterior, the reticular nucleus, and the pars ventralis of the lateral geniculate nucleus. No sign of A:'~~~~~~~~~~~~~~~PSSG B 8 B 9 B7 B11 X(<~~~~~~~~~~~~~~~33 36 Text-fig. 1. The course of the degenerating fibres from a lesion in the middle part of the suprasylvian gyrus (B3) to the cingulate cortex. The lesions (B6-11) surrounding the mid-suprasylvian gyrus caused little or no fibre degeneration in the allocortex. All text- figures and plates refer to cat brains unless otherwise stated. retrograde thalamic degeneration was recognized in these Nauta preparations. Further back there was dense fibre degeneration in the pretectum, and deep in the superior colliculus, and also in the anterior pons, especially in the nucleus pontis lateralis of Winkler & Potter (1914, plate XXI). In addition to these widespread projections, there were degenerating fibres distributed in an arc in the white matter lateral and ventral to the splenial sulcus. Some of these fibres ended in the peristriate cortex (area 18) and others in the adjacent cingulate cortex, but there were none in the retrosplenial area of Rose & Woolsey (1948 a). Within the cortex the degeneration was most concentrated at the dorso-medial lip of the ventral bank of the splenial sulcus, where the cingulate and peristriate areas adjoin (Text-fig. 1; PI. 1, fig. 1). The degeneration surrounding the splenial sulcus extended posteriorly from the level of the lesion. Beneath the posterior end of the splenial sulcus, there is a small gyrus separated from the 342 B. G. CRAGG entorhinal area below by the posterior end of the rhinal fissure (see Text-fig. 3; P1. 1, fig. 3). This gyrus does not appear to be separately named, but forms part of the posterior splenial gyrus of Winkler & Potter (1914, plate XX), who treat it as part of area 29 (post-splenialis). It is not, however, included in the retrosplenial area of Rose & Woolsey (1948 a), and has a rather homogeneous structure that is difficult to characterize (PI. 1, fig. 3). The degenerating fibres surrounding the splenial sulcus continued into this part of the posterior splenial gyrus (P1. 1, fig. 2). Only a very small number of fibres entered the dorsal entorhinal cortex. In the brains with unilateral lesions no fibre degeneration was seen in the allocortex of the contra- lateral hemispheres. Lesions in the mid-suprasylvian gyrus thus caused the degeneration of a pro- jection to the cingulate cortex, and lesions have therefore been made in neighbour- ing areas to define the limits of the neocortex contributing to this projection. Two brains (B 6, 7) with lesions of the posterior suprasylvian gyrus (Text-fig. 1) showed only a very small number of degenerating fibres in part of the cingulate cortex, and none in the posterior splenial gyrus. In another brain (B 8) a lesion was made in the anterior part of the lateral gyrus (Text-fig. 1), but although there were many degenerating fibres in the cortex surrounding the anterior end of the splenial sulcus, few penetrated as far back as the cingulate cortex. As shown in Text-fig. 1, the anterior part of the suprasylvian gyrus was damaged in B 9.
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