The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex

Extracellular recordings were obtained from single neurons in ventrobasal ( VB) thalamus of awake rabbits while field potentials were recorded at vario us depths within topographically aligned and nonaligned barrel columns of s omatosensory cortex (S1). Spike-triggered averages of cortical field potent ials were obtained following action potentials in thalamic neurons. Action potentials in a VB neuron elicited a cortical response within layer 4 with three distinct components. 1) A biphasic, initially positive response (late ncy <1 ms) was interpreted to reflect activation of the VB axon terminals ( the AxTP). This response was not affected by infusion of an alpha-amino-3-h ydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptor antagonis t within the barrel. In contrast, later components of the response were com pletely eliminated and were interpreted to reflect focal synaptic potential s. 2) A negative potential [focal synaptic negativity (FSN)] occurred at a mean latency of 1.65 ms and lasted similar to 4 ms. This response had a rap id rise time (similar to 0.7 ms) and was interpreted to reflect monosynapti c excitation. 3) The third component was a positive potential (the FSP), wi th a slow rise time and a half-amplitude duration of similar to 30 ms. The FSP showed a weak reversal in superficial cortical layers and was interpret ed to reflect di/polysynaptic inhibition. The amplitudes of the AxTP, the F SN, and the FSP reached a peak near layer 4 and were highly attenuated in b oth superficial and deep cortical layers. All components were attenuated or absent when the cortical electrode was missaligned from the thalamic elect rode by a single cortical barrel. Deconvolution procedures revealed that th e autocorrelogram of the presynaptic VB neuron had very little influence on either the amplitude or duration of the AxTP or the FSN, and only a minor influence (mean, 11%) on the amplitude of the FSP. We conclude that individ ual VB thalamic impulses entering a cortical barrel engage both monosynapti c excitatory and di/polysynaptic inhibitory mechanisms. Putative inhibitory interneurons of an S1 barrel receive a highly divergent/convergent monosyn aptic input from the topographically aligned VB barreloid, and this results in sharp synchrony among these interneurons. We suggest that single-fiber access to disynaptic inhibition is facilitated by this sharp synchrony, and that the FSP reflects a consequent synchronous wave of feed-forward inhibi tion within the S1 barrel.