An electron microscopic study of the centre-median and ventrolateral nuclei of the thalamus in the monkey

Abstract

An electron microscopic study has been made of the normal ventrolateral and centre-median nuclei of the thalamus of the monkey and, in experimental material, of the mode of termination in the nuclei of afferent fibres from the motor cortex, the globus pallidus and the deep cerebellar nuclei. There are striking similarities but also a few subtle differences in the ultrastructure of the centre-median and ventrolateral nuclei. Three classes of cell are present: a large multipolar cell with much cytoplasm filled with many organelles is probably the relay cell; a small fusiform cell with a thin rim of cytoplasm and light vacuolated mitochondria, which may contain discoid vesicles, gives rise to P profiles and axon initial segments; the third type is intermediate between the other two in size and other features. There are four types of vesicle-containing synaptic profiles. The most frequent are SR axon terminals, which are small, with spherical synaptic vesicles and are pre-synaptic at asymmetrical contacts with small and medium dendrites and their spines and P profiles; SR terminals are found mainly in the interglomerular neuropil. LR terminals, the largest synaptic profiles, are found in all glomeruli; they contain many round synaptic vesicles and form numerous asymmetrical synapses, being presynaptic to the main dendrite and all its spines and many of the P profiles in a glomerulus. P profiles are irregular pale processes, which occur in considerable numbers outside and within glomeruli (70% of intra-glomerular profiles) and contain pleomorphic synaptic vesicles which are discoid. They arise from tiny unmyelinated profiles and they may have synaptic interaction in several glomeruli. Larger processes, similar in character to proximal dendrites, but with discoid vesicles and synaptic features like those of smaller P profiles are also found, and may be in continuity with a cell soma. P profiles are post-synaptic to LR, SR and F axons, both pre- and postsynaptic to other P profiles and pre-synaptic to conventional dendrites; there are reciprocal synapses between pairs of P profiles. F axons, the least common profiles, are usually extra-glomerular and synapse with proximal dendrites and cell somata; they contain cylindrical synaptic vesicles and are pre-synaptic to P profiles and dendrites at symmetrical synapses. Cell somata in the centre-median nucleus possess spines, and in both nuclei dendrites have spines, both in glomeruli and the neuropil. Multivesicular bodies are frequently present in the parent dendrite subjacent to the spine. Spines in the neuropil are post-synaptic to SR and P profiles and, in the centre-median nucleus, also to F axons. Some spines appear to be post-synaptic only to F axons. At least half the extraglomerular spines are associated with two synapses, a dyadic arrangement with one synapse on the spine and one on the parent dendrite close to the base of the spine, while many dyads have only a single presynaptic profile. Some spines have a more complex synaptology including serial synapses and triads. In glomeruli, spines are always post-synaptic to the LR bouton and always dyadic as the LR terminal also contacts the dendritic shaft close to the base of the spine. Spines account for half the contacts between an LR terminal and the main dendrite in a glomerulus. Glomeruli are found in both nuclei and serial sections have shown the multiplicity of profiles and the complexity of synaptic organization within them. Each glomerulus contains one LR bouton, one main dendrite, and a large number of P profiles, with an occasional SR or F axon terminal at the periphery of the aggregation. The dendrites are of medium calibre, often with several spines, around which the other profiles are situated. An analysis is presented of the profiles and synaptic arrangements in thirty glomeruli from the centre-median and ventrolateral nuclei, with a reconstruction of one large glomerulus. The LR bouton makes numerous synaptic contacts with the main dendrite, half the contacts being upon spines, and a considerable number with P profiles. The latter also have many synapses, being approximately equally pre-synaptic to P profiles and the main dendrites. Various specific types of synaptic array are present within the glomeruli: serial synapses; sequential arrays, where the third profile of a serial synapse is again pre-synaptic; reciprocal synapses; triads which are similar to serial synapses but with an additional contact, profile 1 also being pre-synaptic to profile 3. The complexity of the glomerular synaptology is accentuated by the overlapping of several different types of synaptic array in a given glomerulus. Afferent fibres from the motor cortex and globus pallidus terminate in both nuclei as SR boutons, and in the ventrolateral nucleus the mode of termination of both groups of fibres is very similar. In the centre-median nucleus the terminals of fibres from the cortex have a higher proportion of multisynaptic contacts, are more frequently pre-synaptic to P profiles, and the dendrites upon which they end are less often in receipt of other synapses. The termination of fibres from the globus pallidus in the centre-median nucleus differs from terminals of fibres from the cortex and globus pallidus in the ventrolateral nucleus in being pre-synaptic to fewer P profiles. When the somatic sensory cortex was destroyed as well as the motor area degenerating axon terminals were present in the ventroposterior nucleus; their mode of termination was similar to those in the ventrolateral nucleus, but they were far greater in number. Axons from the cerebellar deep nuclei end in the ventrolateral nucleus as LR boutons within glomeruli. There was no evidence of degeneration in the centre-median nucleus after damage of the cerebellum.

Three-dimensional analysis of cerebellar terminals and their postsynaptic components in the ventral lateral nucleus of the cat thalamus

“…with previous data obtained in the cat (Rinvik and Grofova, 197413;Kultas-Ilinsky et al, 1980a,b, 1985, monkey (Harding, 197313;Harding and Powell, 1977;Kultas-Ilinsky and Ilinsky, 1991), and rat (Aumann et al, 1994). Labeled CTs were distributed mainly on primary and secondary dendrites, but never on cell bodies of TCNs in the present study, and this finding was further confirmed by computerassisted three-dimensional reconstructions of dendrites of single HRP-filled TCNs in the VL (Sato et al, 1992).…”

Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: Single axon reconstructions and immunohistochemical study

“…They found that these degenerated terminals made symmetric synaptic contacts with dendrites and contained pleomorphic vesicles and clusters of mitochondria. On the other hand, the situation is less clear with respect to the MPG/GPi projection, which is presumed to be a homologous structure to the SNR (Harding and Powell, 1977;Finkelstein et al, 1996).…”

Ramification and termination of single axons in the cerebellothalamic pathway of the rat

“…There are a number of studies across different species which have detailed the ultrastructure of cerebellothalamic synapses in the relay nuclei (Rinvik and Grofova, 1974;Harding and Powell, 1977;Ilinsky, 1990;Aumann et al, 1994). They are characterised by their large size, extensively perforated synaptic densities and their proximal location, all of which reflect secure and powerful transmission (Uno et al, 1970;Shinoda et al, 1985a;Sawyer et al, 1994).…”