A comparative analysis of coordinated neuronal activity in the thalamic ventrobasal complex of rats and cats

Abstract

There are substantial differences in the incidence of inhibitory neurons in the ventrobasal complex of rat and cat thalamus. This marked dissimilarity in neuronal composition suggests that there should be corresponding differences in the orchestration of neural activity in these regions during cutaneous stimulation. To explore this possibility, we conducted a cross-correlation analysis of neuronal activity in the ventroposterolateral (VPL) nucleus of anesthetized rats and cats. Pairs of neurons representing hairy skin were recorded simultaneously with one or two electrodes during air jet stimulation of multiple sites throughout the receptive fields. Cross-correlation histograms indicated that correlated activity among adjacent neurons occurred in three distinct patterns. In one pattern, classified as narrow-unimodal, the discharge of one neuron preceded a discharge in the partner neuron over a narrow interval of time (<5 ms). Narrow-bimodal patterns were characterized by responses in which the temporal order of discharges from the two neurons was variable, but the interspike intervals were always <5 ms. In wide-unimodal patterns, the discharge of one neuron was correlated with subsequent discharges in the partner neuron over a wide interval of time (>5 ms). In rat VPL, two-thirds of the 58 neuron pairs showing correlated responses were characterized by narrow-unimodal responses and nearly one-third of the neuron pairs displayed narrow-bimodal patterns. Only one pair of rat VPL neurons were characterized by a wide-unimodal pattern of coordination. By comparison, half of the 61 adjacent neuron pairs with coordinated responses in cat VPL were characterized by narrow-unimodal patterns. Slightly more than one-third of the correlated neuron pairs had narrow-bimodal patterns, while the remainder (13%) were classified as wide-unimodal responses. Pairs of neurons separated by 340–405 μm discharged synchronously in a pattern that was similar to the temporal relationship expressed in the narrow-bimodal patterns found among adjacent neurons. In both species, the wide-unimodal patterns had the strongest coordinated responses as measured by the correlation coefficient. Although inhibitory relationships did not appear in correlation histograms that had been correlated for stimulus coordination, cross-correlation analysis of the raw spike trains revealed brief (10–40 ms) periods of inhibition that were associated with cat VPL neurons exhibiting wide-unimodal coordination patterns. In rat VPL, most inhibition involved longer (30–60 ms) periods of inhibitory oscillations appearing amidst a much larger rhythmic pattern. These results suggest that correlation patterns transpiring over narrow (<5 ms) time intervals represent the coordination of activity among neighboring thalamocortical relay neurons. By contrast, wide-unimodal patterns appear to represent coordinated activity between a thalamocortical relay cell and an intrinsic inhibitory neuron.