The human thalamic somatic sensory nucleus [ventral caudal (Vc)] shows neuronal mechanoreceptor-like responses to optimal stimuli for peripheral mechanoreceptors

Abstract

Although the response of human cutaneous mechanoreceptors to controlled stimuli is well studied, it is not clear how these peripheral signals may be reflected in neuronal activity of the human CNS. We now test the hypothesis that individual neurons in the human thalamic principal somatic sensory nucleus [ventral caudal (Vc)] respond selectively to the optimal stimulus for one of the four mechanoreceptors. The optimal stimuli for particular mechanoreceptors were defined as follows: Pacinian corpuscles (PC), vibration at 128 Hz; rapidly adapting (RA), vibration at 32 or 64 Hz; slowly adapting type 1 (SA1), edge; slowly adapting type 2 (SA2), skin stretch. Nineteen neurons had a significant response to at least one optimal stimulus, and 17 had a significantly greater response to one stimulus than to the other three, including 7 PC-related, 7 RA-like, 3 SA1-like, and 2 SA2-like neurons. One of each of the SA1- and SA2-like thalamic neurons responded to vibration with firing rates that were lower than those to edge or stretch but not significantly. Except in the case of PC-related neurons, the receptive field (RF) sizes were larger for these thalamic neurons than for the corresponding mechanoreceptor. Von Frey thresholds were higher than those for the corresponding human RA and SA1 mechanoreceptors. These results suggest that there is a convergence of pathways transmitting input from multiple mechanoreceptors of one type on single thalamic neurons via the dorsal columns. They are also consistent with the presence of primate thalamic elements of modality and somatotopic isorepresentation.

FIG. 1.

Physiologic characteristics of Pacinian corpuscles (PC)-related thalamic neurons. A: figurines of the receptive field (RF) and projected field (PF). B: response to step indentation and vibration at 32–128 Hz as measured by the Chubbuck stimulator (as labelled). C: entrainment of neuronal firing: top panel, spike trains that signal to the Chubbuck; middle and bottom panels cycle histograms, frequencies as indicated. D: skin stretch, directions as indicated.

FIG. 2.

Physiologic characteristics of rapidly adapting (RA)-like neuron. Conventions as for Fig. 1, A–D. E: skin stretch proximal-distal (P-D) direction above stretch medio-lateral (M-L).

FIG. 3.

Physiologic characteristics of slowly adapting type 1 (SA1)-like neuron. Conventions as for Fig. 2.

FIG. 4.

Physiologic characteristics of SA1-like neuron (neuron 3). Conventions as for Fig. 2.

FIG. 5.

Map of the estimated neuronal location by mechanoreceptor-like classification as in the inset. The calibration bar is 3 mm.