Thalamic projections to sensorimotor cortex in the macaque monkey: Use of multiple retrograde fluorescent tracers

Abstract

We used several fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine Latex Microspheres, Evans Blue, and Fluoro-Gold) in each of eight macaques, to examine the patterns of thalamic input to the sensorimotor cortex of macaques 12 months or older. Inputs to different zones of motor, premotor, and postarcuate cortex, supplementary motor area, and areas 3b/1 and 2/5 in the postcentral cortex, were examined. Coincident labeling of thalamocortical neuron populations with different dyes (1) increased the precision with which their soma distributions could be related within thalamic space, and (2) enabled the detection by double labeling, of individual thalamic neurons that were common to the thalamic soma distributions projecting to separate, dye-injected cortical zones. Double-labeled thalamic neurons projecting to sensorimotor cortex were rarely seen in mature macaques, even when the injection sites were only 1-1.5 mm apart, implying that their terminal arborizations were quite restricted horizontally. By contrast, separate neuron populations in each thalamic nucleus with input to sensorimotor cortex projected to more than one cytoarchitecturally distinct cortical area. In ventral posterior lateral (oral) (VPLo), for example, separate populations of cells sent axons to precentral medial, and lateral area 4, medial premotor, and postarcuate cortex, as well as to supplementary motor area. Extensive convergence of thalamic input even to the smallest zones of dye uptake in the cortex (approximately 0.5 mm3) characterized the sensorimotor cortex. The complex forms of these projection territories were explored using 3-dimensional reconstructions from coronal maps. These projection territories, while highly ordered, were not contained by the cytoarchitectonic boundaries of individual thalamic nuclei. Their organization suggests that the integration of the diverse information from spinal cord, cerebellum, and basal ganglia that is needed in the execution of complex sensorimotor tasks begins in the thalamus.

Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output

“…The origin of this variability is unclear, but it does not appear to be correlated with experimental factors such as survival time, total volume of virus injected, or number of sites injected. More importantly, similar variations have been observed in other studies that used conventional tracers to define origin of thalamic projections to the SMA (Schell and Strick, 1984;Wiesendanger and Wiesendanger, 1985a;Darian-Smith et al, 1990;Rouiller et al, 1994Rouiller et al, , 1999Shindo et al, 1995;Matelli and Luppino, 1996;Sakai et al, 1999Sakai et al, , 2002. In particular, the ratio of neurons labeled in basal ganglia recipient nuclei of the thalamus (VLo, VApc, VLm, VLcr) to neurons labeled in cerebellar recipient nuclei (X, …”

“…The SMA has been considered to be an important target of basal ganglia output (Schell and Strick, 1984;Wiesendanger and Wiesendanger, 1985a;Alexander et al, 1986;Darian-Smith et al, 1990;Rouiller et al, 1994Rouiller et al, , 1999Shindo et al, 1995;Matelli and Luppino, 1996;Sakai et al, 1999Sakai et al, , 2002. In addition, Wiesendanger and Wiesendanger (1985a,b) provided some evidence for cerebellar input to the SMA, especially to its rostral portion, which is now recognized as the pre-SMA.…”

Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys

“…A similar method has been used to compare the relative strength of thalamic inputs to different cortical areas (e.g. Matelli et al, 1989;Darian-Smith et al, 1990;Hatanaka et al, 2003;Morel et al, 2005). Moreover, as the number of labeled neurons in thalamus was relatively low, the use of a stereological probe to estimate their number was not appropriate and therefore we counted all labeled neurons.…”

Functional involvement of the cerebral cortex following paramedian bithalamic infarction

“…Neuroanatomically, there are dense connections between thalamus and the primary sensory cortex (Darian-Smith & Darian-Smith, 1993), as well as between thalamus and primary motor cortex (Darian-Smith, Darian-Smith, & Cheema, 1990). It has been hypothesised (Liepert et al, 2005) that sensory output could have, physiologically, an inhibitory or excitation-limiting effect on the motor cortex.…”