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The termination of strio-pallidal and strio-nigral fibres
125
BRAIN RESEARCH
Short Communications The termination of strio-pallidal and strio-nigral fibres In a recent electron microscopic study of the substantia nigra in the cat, no evidence was found of degenerating terminals after damage of the cortex and the question of the subcortical origin of the numerous axon terminals in the nucleus was raised 8. As part of an analysis of the intrinsic and extrinsic connections of the caudate nucleus some information has been obtained on the termination of the strio-pallidal and strio-nigral fibres. All afferent fibres to the caudate nucleus from the cortex, thalamus and midbrain have terminals with asymmetrical membrane thickenings (Gray, Type 11,4), mainly on spines and dendrites but in the case of cortical fibres, also on cell bodies 6. After lesions within the caudate nucleus there is also degeneration of terminals with symmetrical membrane thickenings (Gray Type I11,4) in the nucleus, in contact with cell somata, dendritic processes and the initial segments of axons. All neurones in the caudate nucleus have axon collaterals 7 and these terminals with symmetrical membrane thickenings could be either of axons which are intrinsic or of collateral branches of efferent axons. In an attempt to distinguish between these possibilities the mode of termination of the striatal efferent fibres in the globus pallidus and substantia nigra have been studied after lesions of various sizes had been placed stereotaxically in the head of the caudate nucleus in adult cats. After a survival of 4 days, the brains were fixed by perfusion with a modified Karnovsky 5 fixative (4~o formaldehyde, 1 ~ glutaraldehyde). Blocks from the globus pallidus and rostro-medial substantia nigra were post-fixed in 2 ~ osmium tetroxide and embedded in Araldite. Thin sections were stained with uranyl acetate and lead citrate. There is a striking similarity in the ultrastructure of the globus pallidus and substantia nigra 9. Neither nucleus has a large number of nerve cells. The dendritic shafts branch infrequently and lack typical spines though an occasional small projection is present with cytoplasm denser than that of the parent dendrite (Fig. 5). There is a high concentration of axon terminals and the dendrites are studded with them 3; the complex thus formed is ensheathed with glia 8 (Fig. 1). Axosomatic synapses are less common, but the cell bodies have a tight glial wrapping absent only at the regions of synaptic contact where the glial processes frequently lie over the axon terminal. Most endings have symmetrical membrane thickenings and presynaptic dense projections are frequent. Terminals with asymmetrical synaptic thickenings are also present and both types are in contact with somata, and dendrites and their projections. Varicose dendrites are common in the globus pallidus (Fig. 3). Following a lesion in the caudate nucleus degenerating axosomatic and axodendritic terminals with symmetrical synaptic thickenings were seen in the globus pallidus (Figs. 2 and 5) and substantia nigra (Figs. 6 and 7). In some regions of the globus paIIidus the degeneration was particularly dense, dendrites being surrounded by dark profiles (Fig. 4). A degenerating terminal with an asymmetrical membrane Brain Research, 17 (1970) 125-128
Fig. 1. Substantia nigra. Dendrites with nunaerous terminals and glial wrapping. 2].~1~), Fig. 2. Globus pallidus. Degenerating terminal onto large dendrite. :, 30,q00. Fig. 3. Globus pallidus. Varicose dendrite with many synapses. 7,700. Abbreviations used in these and subsequent figures: D, dendrite; G, gila: P, dendrint ~3rojection, Heavy arrows, degenerating terminals: light ~rrows. degenerating preterminals: art~w heads, glial sheath.
Fig. 4. Globus pallidus. Dendrite surrounded by degenerating tern.inals. : 29,100. Fig. 5. Globus pallidus. Dendrite, associated ~vith terminal and preterminal degeneration, with small pro iection. 24,300. Fig. 6. Substantia nigra. Dendrite with degenerating terminals. ,. 29,100. Fig. 7. Substantia nigra. Degenerating ending onto dendrite, x 32,000.
128
SI-tORT (~OMMUNI(AFIONS
thickening was seen occasionally in the pallidum in one brain with a large lesion where there had been some involvement of white matter. The m a j o r outflow from the striatum is to the globus pallidus with a smaller projection to the s u b s t a n t i a nigra ~° and it is interesting to find that these efferents have terminals with symmetrical m e m b r a n e thickenings in the two nuclei which are so similar in other respects. "Ihe endings with symmetrical m e m b r a n e thickenings in the caudate nucleus which degenerate after damage within the nucleus could therefore be collaterals of the strio-pallidal and strio-nigral axons; in addition there could be n e u r o n e s strictly intrinsic to the caudate with asymmetrical or symmetrical synaptic thickenings. W h e t h e r the terminals with symmetrical m e m b r a n e thickenings have the same functional significance, as has been suggested in other regions ~l" the brain ~, remains to be investigated. This work was supported by a grant from the Medical Research Council. Department of Human Anatomy, University of Oxford, Oxford (Great Britain)
JANET M. KEMP
1 COLONNIER,M., Synaptic patterns in different cell types in the different laminae of the cat visual cortex. An electron microscope study, Brain Research, 9 (1968) 268-287. 2 ECCLES,J. C., The Physiology of Synapses, Springer, Berlin, 1964. 3 Fox, C. A., HILLMAN,D. E., SIEGESMUND,K. A., ANDSETHER,L. A., The primate gtobus pallidus and its feline apd avian homologues: a Golgi and electron microscopic study. In R. HASSLERAND H. STEPrIAN(Eds.), Evolution of the Forebrain, Thieme, Stuttgart, 1966, pp. 237-248. 4 GRAY,E. G., Axosomatic and axodendritic synapses of the cerebral cortex : an electron microscope study, J. Anat. (lond.), 93 (1959) 420-433. 5 KAR~OVSKY,M. J., A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy, J. Cell Biol., 27 (1965) 137A. 6 KEMP, J. M., An electron microscopic study of the termination of afferent fibres in the caudate nucleus, Brain Research, 11 (1968) 464-467. 7 KEMP,J. M., Observations on the caudate nucleus of the cat impregnated with the Golgi method, Brain Researeh, 11 (1968) 467470. 8 RINVIK,E., AND WALBERG,F., ls there a cortico-nigral tract? A comment based on experimental electron microscopic observations in the cat, Brain Research, 14 (1969) 742-744. 9 SCHWYN,R. C., AND FOX, C. A., A Golgi and electron microscopic study of the substantia nigra in Maeaca mulatta and Saimiri schtreus, Anat. Rec., 163 (1969) 342. 10 SZABO,J., Tor~ical distribution of striatal efferents in the monkey, Exp. Neurol_ 5 (1962) 21-36. (Accepted October 22nd, 1969)
Brain Research, 17 (1970) 125-128
BRAIN RESEARCH
Short Communications The termination of strio-pallidal and strio-nigral fibres In a recent electron microscopic study of the substantia nigra in the cat, no evidence was found of degenerating terminals after damage of the cortex and the question of the subcortical origin of the numerous axon terminals in the nucleus was raised 8. As part of an analysis of the intrinsic and extrinsic connections of the caudate nucleus some information has been obtained on the termination of the strio-pallidal and strio-nigral fibres. All afferent fibres to the caudate nucleus from the cortex, thalamus and midbrain have terminals with asymmetrical membrane thickenings (Gray, Type 11,4), mainly on spines and dendrites but in the case of cortical fibres, also on cell bodies 6. After lesions within the caudate nucleus there is also degeneration of terminals with symmetrical membrane thickenings (Gray Type I11,4) in the nucleus, in contact with cell somata, dendritic processes and the initial segments of axons. All neurones in the caudate nucleus have axon collaterals 7 and these terminals with symmetrical membrane thickenings could be either of axons which are intrinsic or of collateral branches of efferent axons. In an attempt to distinguish between these possibilities the mode of termination of the striatal efferent fibres in the globus pallidus and substantia nigra have been studied after lesions of various sizes had been placed stereotaxically in the head of the caudate nucleus in adult cats. After a survival of 4 days, the brains were fixed by perfusion with a modified Karnovsky 5 fixative (4~o formaldehyde, 1 ~ glutaraldehyde). Blocks from the globus pallidus and rostro-medial substantia nigra were post-fixed in 2 ~ osmium tetroxide and embedded in Araldite. Thin sections were stained with uranyl acetate and lead citrate. There is a striking similarity in the ultrastructure of the globus pallidus and substantia nigra 9. Neither nucleus has a large number of nerve cells. The dendritic shafts branch infrequently and lack typical spines though an occasional small projection is present with cytoplasm denser than that of the parent dendrite (Fig. 5). There is a high concentration of axon terminals and the dendrites are studded with them 3; the complex thus formed is ensheathed with glia 8 (Fig. 1). Axosomatic synapses are less common, but the cell bodies have a tight glial wrapping absent only at the regions of synaptic contact where the glial processes frequently lie over the axon terminal. Most endings have symmetrical membrane thickenings and presynaptic dense projections are frequent. Terminals with asymmetrical synaptic thickenings are also present and both types are in contact with somata, and dendrites and their projections. Varicose dendrites are common in the globus pallidus (Fig. 3). Following a lesion in the caudate nucleus degenerating axosomatic and axodendritic terminals with symmetrical synaptic thickenings were seen in the globus pallidus (Figs. 2 and 5) and substantia nigra (Figs. 6 and 7). In some regions of the globus paIIidus the degeneration was particularly dense, dendrites being surrounded by dark profiles (Fig. 4). A degenerating terminal with an asymmetrical membrane Brain Research, 17 (1970) 125-128
Fig. 1. Substantia nigra. Dendrites with nunaerous terminals and glial wrapping. 2].~1~), Fig. 2. Globus pallidus. Degenerating terminal onto large dendrite. :, 30,q00. Fig. 3. Globus pallidus. Varicose dendrite with many synapses. 7,700. Abbreviations used in these and subsequent figures: D, dendrite; G, gila: P, dendrint ~3rojection, Heavy arrows, degenerating terminals: light ~rrows. degenerating preterminals: art~w heads, glial sheath.
Fig. 4. Globus pallidus. Dendrite surrounded by degenerating tern.inals. : 29,100. Fig. 5. Globus pallidus. Dendrite, associated ~vith terminal and preterminal degeneration, with small pro iection. 24,300. Fig. 6. Substantia nigra. Dendrite with degenerating terminals. ,. 29,100. Fig. 7. Substantia nigra. Degenerating ending onto dendrite, x 32,000.
128
SI-tORT (~OMMUNI(AFIONS
thickening was seen occasionally in the pallidum in one brain with a large lesion where there had been some involvement of white matter. The m a j o r outflow from the striatum is to the globus pallidus with a smaller projection to the s u b s t a n t i a nigra ~° and it is interesting to find that these efferents have terminals with symmetrical m e m b r a n e thickenings in the two nuclei which are so similar in other respects. "Ihe endings with symmetrical m e m b r a n e thickenings in the caudate nucleus which degenerate after damage within the nucleus could therefore be collaterals of the strio-pallidal and strio-nigral axons; in addition there could be n e u r o n e s strictly intrinsic to the caudate with asymmetrical or symmetrical synaptic thickenings. W h e t h e r the terminals with symmetrical m e m b r a n e thickenings have the same functional significance, as has been suggested in other regions ~l" the brain ~, remains to be investigated. This work was supported by a grant from the Medical Research Council. Department of Human Anatomy, University of Oxford, Oxford (Great Britain)
JANET M. KEMP
1 COLONNIER,M., Synaptic patterns in different cell types in the different laminae of the cat visual cortex. An electron microscope study, Brain Research, 9 (1968) 268-287. 2 ECCLES,J. C., The Physiology of Synapses, Springer, Berlin, 1964. 3 Fox, C. A., HILLMAN,D. E., SIEGESMUND,K. A., ANDSETHER,L. A., The primate gtobus pallidus and its feline apd avian homologues: a Golgi and electron microscopic study. In R. HASSLERAND H. STEPrIAN(Eds.), Evolution of the Forebrain, Thieme, Stuttgart, 1966, pp. 237-248. 4 GRAY,E. G., Axosomatic and axodendritic synapses of the cerebral cortex : an electron microscope study, J. Anat. (lond.), 93 (1959) 420-433. 5 KAR~OVSKY,M. J., A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy, J. Cell Biol., 27 (1965) 137A. 6 KEMP, J. M., An electron microscopic study of the termination of afferent fibres in the caudate nucleus, Brain Research, 11 (1968) 464-467. 7 KEMP,J. M., Observations on the caudate nucleus of the cat impregnated with the Golgi method, Brain Researeh, 11 (1968) 467470. 8 RINVIK,E., AND WALBERG,F., ls there a cortico-nigral tract? A comment based on experimental electron microscopic observations in the cat, Brain Research, 14 (1969) 742-744. 9 SCHWYN,R. C., AND FOX, C. A., A Golgi and electron microscopic study of the substantia nigra in Maeaca mulatta and Saimiri schtreus, Anat. Rec., 163 (1969) 342. 10 SZABO,J., Tor~ical distribution of striatal efferents in the monkey, Exp. Neurol_ 5 (1962) 21-36. (Accepted October 22nd, 1969)
Brain Research, 17 (1970) 125-128