Spatiotemporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus

Abstract

Classically, the rat ventral posterior medial (VPM) nucleus of the thalamus has been considered as a simple passive relay for single-whisker information to the primary somatosensory cortex (SI). However, recent reports have suggested that the VPM could contain a much more coarsely coded and spatiotemporally complex representation of the rat whisker pad. To address this possibility properly, we have carried out chronic simultaneous recordings of large numbers (up to 23) of single neurons, distributed across the entire VPM, in both awake and lightly anesthetized adult rats. Quantitative, computer-based reconstruction of receptive fields (RFs) revealed that single VPM neurons exhibit significant responses to discrete stimulation of as many as 20 single whiskers (mean ± SD RF size, 13.7 ± 4.8 whiskers). By defining multiple response magnitude (RM) thresholds it was possible to subdivide these large VPM RFs quantitatively into a prominent center (mean ± SD, 1.41 ± 0.70 whiskers, RM > 95%) and an excitatory surround (up to 18 whiskers, RM < 95%). VPM neurons exhibited both short- latency responses (SLRs, from 4 to 10 msec poststimulus) and/or long-latency responses (LLRs, 15-25 msec), each followed by inhibitory responses. Though LLRs were weaker (mean ± SD, 47.19 ± 33.34 Hz) than SLRs (119.63 ± 50.12 Hz), they often defined RFs that differed considerably from those defined by the SLRs of the same cell. In particular, VPM cells with short-latency RFs centered in caudal whiskers (e.g., C1, D1, E1) showed a poststimulus time- dependent shift of these RF centers toward the rostral whiskers (e.g., C4, D4, E4). These caudal-to-rostral (C→R) RF shifts occurred in neurons with the largest RFs of our sample (17.2 ± 2.4 whiskers). On the other hand, VPM cells with short-latency RFs centered in rostral whiskers had the smallest RFs (13.1 ± 4.1 whiskers) and usually did not exhibit time-dependent RF center shifts. Multivariate analysis revealed that these two groups of VPM neurons, C→R shifting and rostral position (RP) cells, could be statistically distinguished according to a combination of three RF attributes (short-latency RF center location, RF size, and magnitude of RF center shift). Quantitative, computer-based reconstruction of 'population response maps' demonstrated that the 'place' coding for each single whisker in the VPM involved a distinct weighted contribution from a large proportion of the simultaneously recorded neurons. Furthermore, single-whisker stimulation induced a complex spatiotemporal wave of sensory-evoked activity that involved a much larger area of the VPM than a single barreloid, the classical anatomical representation of a single whisker in this nucleus. These results argue against the classical view that the rat VPM contains a highly topographic representation of single facial whiskers. Instead, they suggest that somatosensory information is processed in a much more distributed manner by ensembles of functionally heterogeneous populations of VPM neurons. Our hypothesis is that spatiotemporally complex multiwhisker RFs in the VPM emerge from asynchronous convergence of multiple ascending and descending afferents. As such, the functional properties of the VPM observed here may reflect dynamic processing of sensory information at multiple levels of the somatosensory network.