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Strio-Pallidal Projection in the Monkey

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Strio-Pallidal Projection in the Monkey J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.5.426 on 1 October 1966. Downloaded from J. Neurol. Neurosurg. Psychiat., 1966, 29, 426 Strio-pallidal projection in the monkey W. M. COWAN AND T. P. S. POWELL From the Department of Human Anatomy, University of Oxford The corpus striatum in the mammalian brain appears firmation of the organization of strio-pallidal and to receive only two major groups of afferents: from strio-nigral connexions, but also because they the intralaminar nuclei of the thalamus and from demonstrate the value of the study of the distribu- most areas of the cerebral cortex. A common feature tion ofgliosis as an analytical method in fibre systems of both groups of afferents is their well-developed in which the direction of conduction is known. topographical organization. Rostral and caudal The organized nature of the afferent and efferent parts of the thalamus and cortex are related to the connexions of the striatum has assumed greater corresponding parts of the striatum (Powell and significance with the demonstration by Nauta and Cowan, 1956; Webster, 1961, 1965; Carman, Cowan, Mehler (1966) that the small-celled external segment and Powell, 1963); in the medio-lateral dimension of the globus pallidus sends fibres only to the sub- the organization is more complex, and does not thalamic nucleus, whereas the large-celled inner conform, as might have been supposed, to the simple segment is related to the thalamus and midbrain.guest. Protected by copyright. division of the striatum into a medial caudate Their additional finding that part of the projection nucleus and a laterally placed putamen. Instead, the from the internal segment is to the centromedian available evidence suggests that the efferents from nucleus is of particular interest: first, because it may the greater part of the cerebral cortex and most of provide a 'circular pathway' from the striatum to the the intralaminar nuclei terminate on both sides of globus pallidus and thalamus, and back to the the internal capsule. Thus, for example, in the rabbit striatum; second, because of the substantial projec- the cortex on the dorso-lateral surface of the hemi- tion to the intralaminar nuclei of the thalamus sphere sends fibres both to the caudate and putamen (including the centromedian nucleus) from the (Carman et a!., 1963), and in the monkey, following cerebral cortex (Auer, 1956; Niimi, Kishi, Miki, a lesion in the centromedian nucleus degenerating and Fujita, 1963; Astruc, 1964; Petras, 1964; fibres can be traced into both the caudate and Mehler, 1966; Powell and Cowan, 1966). putamen (Mehler, 1966). In the present paper, on the basis of our own and In view of this evidence it was of some interest to other workers' findings on the strio-pallidal projec- determine whether the functional organization tion, an attempt will be made to synthesize some of imposed upon the architectonically homogeneous the recent anatomical work on the inter-relationships striatum by its afferents is reflected also in its between the cerebral cortex, thalamus, and the strio- efferent connexions. Our attention was drawn to this pallidum. question several years ago when studying the thalamo-striate connexions (Powell and Cowan, MATERIAL AND METHODS http://jnnp.bmj.com/ 1956) because in most of the material used in that study discrete areas of intense gliosis were observed The brains of 28 monkeys (Macaca mulatta) were avail- in different parts of the globus pallidus and sub- able for this study (cf. Powell and Cowan, 1956, 1966). stantia nigra with experiments involving varying In 26 of these brains lesions of varying size had been portions of the caudate nucleus and putamen. The placed in either the caudate nucleus or in the putamen. publication in 1960 and 1962 of papers by Voneida The lesions in the putamen were all placed stereotactically and by Szabo on the distribution of striatal efferents with the aid of Olszewski's Atlas (1952). Several of those showed a close correspondence between the pattern in the caudate nucleus were made in the same way, but a on September 24, 2021 by of the projection of the striatum as determined by number were placed under direct vision, through a trans- Nauta method and our own findings on the dis- callosal approach to the lateral ventricle. In a few of the the brains bilateral lesions had been placed, but they were tribution of gliosis in our earlier material and in always in distinctly different parts of the striatum on the several additional brains prepared since that time two sides. The remaining two brains had large neocortical (Powell and Cowan, 1966). It was considered worth- lesions, without involvement of the striatum, and were while, therefore, to put our observations on record used as controls to show that incidental involvement of not only because they provide independent con- cortical projection fibres does not contribute significantly 426 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.5.426 on 1 October 1966. Downloaded from Strio-pallidal projection in the monkey 427 to the gliosis seen in the globus pallidus after striatal gliosis in distinctly different parts of the globus lesions. pallidus. In the brain of monkey OM 21 a narrow The animals were allowed to survive for periods rang- lesion was placed in the ventro-lateral part of the ing from one to four months after operation, following putamen; the damage extends from just behind the which the brains were removed, fixed either in 70% alcohol and 20% acetic acid or in 10 % formalin and rostral end of the putamen back to the level of embedded in paraffin wax. From the serial sections cut junction of its rostral and middle halves (Fig. 1). throughout the extent of the cerebral hemisphere a In the globus pallidus there is a focus of intense regular one-in-five or one-in-ten series was routinely gliosis in the ventral and lateral parts of the external mounted and stained with thionin. segment beginning just behind the caudal limit of the lesion and extending back to about the middle RESULTS of the antero-posterior extent of that segment. The gliosis reaches as far laterally as the junction be- As the lesions in the striatum and the distribution of tween the putamen and globus pallidus, and medially the resulting gliosis in the globus pallidus in several for a short distance into the internal segment; just of the brains are similar both in their site and extent, as its medio-lateral and supero-inferior limits are only a small number of representative experiments sharply defined so it stops quite abruptly over the will be described in detail. The first two experiments space of a few sections at both its rostral and caudal demonstrate that localized lesions, either in the ends. It may be noted that witliin the area of gliosis putamen or in the caudate nucleus, result in heavy there does not appear to be any appreciable change guest. Protected by copyright. OM 21 http://jnnp.bmj.com/ on September 24, 2021 by FIG. 1. Diagram to show the site and extent of the lesion in the putamen in experiment OM 21 and the distribution of the resulting gliosis in the globus pallidus. In this and the subsequent illustrations in which only one lesion is shown, the area of the striatal damage is indicated in solid black and the pallidal gliosis marked by bold arrows andfilled-in circles. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.5.426 on 1 October 1966. Downloaded from 428 W. M. Cowan and T. P. S. Powell Om 18 guest. Protected by copyright. FIG. 2. The lesion in the head of the caudate nucleus together with the pallidal gliosis in experiment OM 18. in the number, size, or staining of the pallidal posteriorly it comes to involve the dorso-lateral part neurones, although, of course, they are more com- of the internal segment. The similarity in the antero- pactly arranged than normal. posterior extent of the gliosis in the pallidum in these http://jnnp.bmj.com/ The findings in this brain may be compared with two brains is almost certainly correlated with the those in experiment OM 18 in which the lesion is fact that the lesions in the two cases are more or less situated in the head of the caudate nucleus. Again, co-extensive in this dimension. In the medio-lateral the damage begins just behind the rostral end of the dimension, on the other hand, there is a distinct caudate as a small, oval area of destruction close to topographical difference in the distribution of the the ventricular margin; further posteriorly the lesion gliosis within the pallidum as a whole. occupies a more lateral position at thejunction of the The next group of six experiments has been middle and medial thirds of the nucleus, but at no selected to illustrate in more detail the principles of on September 24, 2021 by point does it encroach upon the internal capsule the organization of the projection of the putamen (Fig. 2). In the rostral half of the globus pallidus upon the globus pallidus. The site and extent of the there is a dense band of gliosis along the dorso- lesions in the first two of these experiments are medial border of both the external and internal shown in Figure 3. In experiment OM 9 the lesion segments immediately adjoining the internal capsule. occupies a considerable part of the dorso-lateral Anteriorly the gliosis occupies only the dorso-medial region of the putamen from just in front of the corner of the external segment, but when traced middle of its antero-posterior extent back almost to J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.5.426 on 1 October 1966.
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