Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex

Abstract

The ventral posteromedial nucleus (VPM) of the monkey thalamus was investigated with combined immunocytochemical, histochemical, and connection-tracing techniques. Injections of anterogradely transported tracers were placed selectively in the caudal nucleus of the spinal trigeminal nuclear complex, and retrogradely transported horseradish peroxidase (HRP) or fluorescent dyes were placed on the surface or into the depths of defined parts of the trigeminal representation in the first somatic sensory area (SI) of the cerebral cortex. The results are correlated with those of the preceding paper (Rausell and Jones, 1991), which demonstrated the presence of 2 domains in the nucleus on the basis of different patterns of cytochrome oxidase (CO) staining and calcium-binding protein immunoreactivity. The cells of the CO-defined rod and matrix domains receive inputs from different components of the trigeminal afferent system and project to different layers of SI. The large- and medium-sized relay cells of the CO-rich rods, which are immunoreactive for parvalbumin, all project to middle layers of SI. The small relay cells of the weakly-stained CO-matrix, surrounding and intervening between the rods, are immunoreactive for 28-kDa calbindin and project to superficial layers (I and II) of SI. Anterograde tracing studies reveal that the rod domain in VPM is innervated by fibers arising in the contra- and ipsilateral principal trigeminal nucleus, while the matrix domain (and calbindin-positive domains in adjacent nuclei) are innervated by fibers arising in the caudal nucleus of the spinal trigeminal complex. These results demonstrate the modularity and parallel streaming of the functional components of the trigeminal part of the somatic sensory system and suggest that lemniscal and nonlemniscal elements of the system gain access by separate routes to different layers of the SI cortex.

Widespread Thalamic Terminations of Fibers Arising in the Superficial Medullary Dorsal Horn of Monkeys and Their Relation to Calbindin Immunoreactivity

“…1). Enclosed within the lamina are the larger Nissl-stained cells that form the rod domain of the nucleus (Rausell and Jones, 1991a) and smaller cells of the matrix domain of VPM that include the small-celled zone of VPM and the basal ventral medial nucleus (VMb). The aggregated cells of the rods stain intensely for CO and for parvalbumin, and the rods at the medial tip of VPM also costain for calbindin, forming the densest focus of calbindin immunoreactivity in the posterior thalamus (Fig.…”

“…It seems likely that the injections described by Craig et al (1994) were too small and of too limited a rostrocaudal extent to reveal the complex and widespread pattern of projections from lamina I to the thalamus (Jones, 2002;Willis et al, 2002;Ralston, 2003); however, the account of labeled terminations of STT and sVTT axons representing the face, body, and limbs being found exclusively in the calbindin-rich tip of VPM cannot be correct. From mapping studies, the medial tip represents only ipsilateral intraoral structures (Rausell and Jones, 1991a) and projects to primary somatosensory cortex (Manger et al, 1995(Manger et al, , 1996, not to the cingulate region.…”

Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat

“…Because most cortically projecting neurons were found to be PAG ϩ , we concluded that the Calb ϩ cortically projecting neurons most probably contain this enzyme and are thus potentially glutamatergic. Such cells may parallel in their projections and actions the Calb ϩ glutamatergic neurons of the thalamus (Frassoni et al, 1997), which provide a widespread projection to the superficial layers of the cerebral cortex (Rausell and Jones, 1991;Jones, 1998). The vast majority of Calret ϩ neurons was immunopositive for PAG and not retrogradely labeled from the cortex, thus likely corresponding to glutamatergic neurons with caudally or locally directed projections.…”

Calcium binding proteins distinguish large and small cells of the ventral posterior and lateral geniculate nuclei of the prosimian galago and the tree shrew (Tupaia belangeri).

“…Thus, the small cells in VP are not targets of the lemniscal path (11,12), and the small cell layers of GL in galago (layers 4 and 5) receive small fibers from the superior colliculus (SC), which, in turn, is the target of the smallest fibers of the optic tract (3,13). The general principle we seek may simply be that pathways to the superficial layers Abbreviations: GL, lateral geniculate nucleus; Lat, lateral nuclear group; Po, posterior nuclear group; Pul, pulvinar nucleus; SC, superior colliculus; VP, ventral posterior nucleus; VPi, inferior division of the VP; VPs, superior division of the VP.…”

“…In the past few years, Jones and his colleagues (11,12,14) have shown that large and small cells in the thalamus differ in their staining for calcium binding proteins, calbindin and parvalbumin. The clusters of big cells in VP of the monkey are rich in parvalbumin, whereas the small, pale cells in the matrix are rich in calbindin.…”