Functional characteristics of the parallel SI- and SII-projecting neurons of the thalamic ventral posterior nucleus in the marmoset.

The functional organization of the primate somatosensory system at thalamocortical levels has been a matter of controversy, in particular, over the extent to which the primary and secondary somatosensory cortical areas, SI and SII, are organized in parallel or serial neural networks for the processing of tactile information. This issue was investigated for the marmoset monkey by recording from 55 single tactile-sensitive neurons in the lateral division of the ventral posterior nucleus of the thalamus (VPL) with a projection to either SI or SII, identified with the use of the antidromic collision technique. Neurons activated from the hand and distal forearm were classified according to their peripheral source of input and characterized in terms of their functional capacities to determine whether the direct thalamic input can account for tactile processing in both SI and SII. Both the SI- and SII-projecting samples contained a slowly adapting (SA) class of neurons, sensitive to static skin displacement, and purely dynamically sensitive tactile neurons that could be subdivided into two classes. One was most sensitive to high-frequency (> or =100 Hz) cutaneous vibration whose input appeared to be derived from Pacinian sources, while the other was sensitive to lower frequency vibration (< or =100 Hz) or trains of rectangular mechanical pulse stimuli, that appeared to receive its input from rapidly adapting (RA) afferent fibers presumed to be associated with intradermal tactile receptors. There appeared to be no systematic differences in functional capacities between SI- and SII-projecting neurons of each of these three classes, based on receptive field characteristics, on the form of stimulus-response relations, and on measures derived from these relations. These measures included threshold and responsiveness values, bandwidths of vibrational sensitivity, and the capacity for responding to cutaneous vibrotactile stimuli with phase-locked, temporally patterned impulse activity. The analysis indicates that low-threshold, high-acuity tactile information is conveyed directly to both SI and SII from overlapping regions within the thalamic VP nucleus. This direct confirmation of a parallel functional projection to both SI and SII in the marmoset is consistent with our separate studies at the cortical level that demonstrate first, that tactile responsiveness in SII largely survives the SI inactivation and second, that SI responsiveness is largely independent of SII. It therefore reinforces the evidence that SI and SII occupy a hierarchically equivalent network for tactile processing.