Basal ganglia and cerebellum receive different somatosensory information in rats.

Abstract

There are two great subcortical circuits that relay sensory information to motor structures in the mammalian brain. One pathway relays via the pontine nuclei and cerebellum, and the other relays by way of the basal ganglia.We studied the cells of origin of these two major pathways from the posteromedial barrel subfield ofrats, a distinct region ofthe somatosensory cortex that contains the sensory representation of the large whiskers. We itjected tracer substances into the caudate putamen or the pontine nuclei and charted the location of retrogradely filled cortical cells. In preliminary studies, we used double-labeling techniques to determine whether the cells of origin of these two pathways send axon collaterals to other subcortical targets. Lamina V of the rat posteromedial barrel subfield contains two distinct populations of subcortically projecting neurons, which are organized into distinct sublaminae. Corticopontine cells are located exclusively in sublamina Vb, the deeper of two sublaminae revealed by cytochrome oxidase staining. Corticostriate cells are located almost exclusively in the more superficial sublamina Va. Experiments using double-labeling fluorescent tracers demonstrate that about one-quarter of the corticopontine cells send a collateral branch to the superior colliculus. Other studies have shown that cells in Vb are activated at very short latency after vibrissal stimulation; hence, they would seem to be an appropriate relay for the rapid transmission of sensory information to the cerebellum for use in sensory guidance of movement.Sensory areas of the cerebral cortex are connected to motor areas by way of corticocortical circuits and two prominent subcortically directed pathways. One subcortical pathway goes to the basal ganglia, and the other goes to the cerebellum via the pontine nuclei (1-4). The efferent terminals from the basal ganglia and cerebellum remain largely distinct in the thalamus and their thalamic targets project to nonoverlapping regions of the motor cortex (5). Do the basal ganglia and the cerebellum receive inputs from the same or a different population of sensory cortical cells?The great majority of the cells in the sensory cortex that project to these two motor systems are located in lamina V of the cerebral cortex (2, 6-8). Lamina V may be divided into two sublaminae: a superficial sublamina Va and a deep sublamina Vb, which differ in a number of important respects. In mice, lamina Vb receives direct input from the somatosensory relay nucleus in the thalamus; Va does not (9). Stimulation of the appropriate whisker in rats activates cells in sublamina Vb at a latency that is as short as that for activating cells in lamina IV, the principal target of incoming thalamic fibers (10). In contrast, cells in Va respond at much longer latency to such stimulation. Cells in Va stain palely when tested for the presence of the metabolic enzymes cytochrome oxidase or succinic dehydrogenase (11). Cells in sublamina Vb stain far more densely, suggesting that they are capable ofh...

Invited Review Anatomical loops and their electrical dynamics in relation to whisking by rat

“…Note that the primary motor cortex is taken as the parasagittal agranular medial area. (cortex ® superior colliculus) Both sensory and motor cortex send descending projections to the superior colliculus (Wise and Jones, 1977;Killackey and Erzurumlu, 1981;Welker et al, 1988;Mercier et al, 1990). Miyashita and Shigemi (1995) have demonstrated possible cellular interaction between the descending cortical M1 projection to colliculus and the colliculus to facial nucleus projection, consistent with the relay of motor commands to the facial nucleus.…”

“…One involves projections between the forebrain and the cerebellum. Vibrissa S1 cortex sends descending projections to the pons (Kennedy et al, 1966;Wise and Jones, 1977;Shambes et al, 1978;Wiesendanger and Wiesendanger, 1982a, b;Welker et al, 1988;Mercier et al, 1990) whose climbing fiber input to the cerebellum overlaps with that from the trigeminal nuclei (Bower et al, 1981;Morisette and Bower, 1996). Vibrissal M1 cortex also projects to the pons (Wiesendanger and Wiesendanger, 1982a, b;Miyashita et al, 1994).…”

“…Feedback to cortex occurs via projections from the deep cerebellar to ventral lateral thalamic nuclei (Haroian et al, 1981;Gerfen et al, 1982;Deniau et al, 1992;Middleton and Strick, 1997). The second loop involves projections from vibrissa S1 and M1 cortices to basal ganglia (Wise and Jones, 1977;Donoghue and Kitai, 1981;Mercier et al, 1990;L Â evesque et al, 1996). Feedback to cortex occurs via ventral lateral thalamus, as in the case of cerebellar feedback (Fig.…”

Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex

“…The L4-to-L5A connections may form a "short circuit" between afferent signals to the cortex and efferent signals that leave the cortex from layer 5A and project to subcortical regions, for example, the basal ganglia (Mercier et al, 1990;Alloway et al, 1999). The short circuit has the effect that afferent excitation at least potentially bypasses the supragranular layers (layers 2/3 and 1), as illustrated schematically in Figure 7A.…”

Layer V Neurons in Mouse Cortex Projecting to Different Targets Have Distinct Physiological Properties

“…Neurons within layer Va of the barrel cortex project callosally to the contralateral cortex, intracortically to regions including the motor and secondary somatosensory cortex and to the striatum (Bernardo et al 1990;Hoeflinger et al 1995;Koralek et al 1990). The large pyramidal cells of layer Vb have subcortical projections to regions including the posteromedial thalamic nucleus (POm), principle and spinal trigeminal nuclei (Sp5), superior colliculus, pontine nuclei, spinal cord, and striatum (Chmielowska et al 1989;Deschenes et al 1994;Killackey et al 1989;Mercier et al 1990;Wise and Jones 1977a). The properties of identified corticotectal, corticopontine, and callosal cells of the primary visual cortex have been well described in several species.…”