Thalamocortical interactions in the somatosensory system: Interpretations of latency and cross-correlation analyses

1. Isolated extracellular neuronal responses to cutaneous stimulation were simultaneously recorded from corresponding peripheral representations in the ventrobasal nucleus and primary somatosensory cortex of intact, halothane- anesthetized rats. Thalamic and cortical neurons representing hairy skin on the forelimb were activated by hair movements produced by a series of 50 or 100 discrete air jets. A corresponding set of neurons representing the glabrous pads of the hind paw were activated by a similar number of punctate mechanical displacements. 2. Cortical electrode penetrations were histologically reconstructed, and 118 neurons in the glabrous skin representation exhibited cutaneous responses that were categorized into supragranular, granular, or infragranular groups according to their laminar position. Minimum latencies of cortical neurons responding to glabrous skin displacement were analyzed, and significant differences were found in the distribution of minimum latencies for the different cortical layers. Mean values for minimum latencies in the infragranular and granular layers were 15.8 and 16.3 ms. respectively, whereas supragranular neurons were characterized by minimum latencies having a mean of 20 ms. The differences between these groups suggests that stimulus-induced afferent activity reaches infragranular and granular layers before contacting supragranular neurons. Average latencies were also calculated on responses occurring during the 1st 20 trials, but the cortical distributions of these values overlapped considerably, and differences between the laminar groups were not statistically significant. 3. In several recording sites, two cortical neurons were recorded simultaneously, and the response latencies of these matched pairs were often substantially different despite the similarity in laminar position. This result indicates that laminar location is not the only determinant of response latency and that serially organized circuits are distributed within, as well as between, cortical layers. 4. From a sample of 302 neurons exhibiting cutaneous responses within histologically identified regions of thalamus or cortex, a set of 143 pairs of neurons recorded simultaneously from both regions was available for cross-correlation analysis. Significant thalamocortical interactions were found in 38 neuron pairs. Analysis of these significant interactions revealed that thalamocortical connection strength, as measured by neuronal efficacy, was two to four times larger for neuron pairs having the cortical cell in granular layer IV than for neuron pairs having an extragranular layer cortical neuron. There was no difference in thalamocortical connection strength between neuron pairs containing supra- or infragranular cortical neurons. 5. Summed peristimulus time histograms revealed stimulus-locked inhibition of spontaneous activity in 4% (8/195) of cortical and 18% (20/107) of thalamic neurons. A sequence of excitation followed by inhibition was frequently produced by stimulating the center of a neuron's receptive field, but exclusively inhibitory responses were observed when the edge of the neuron's receptive field was stimulated. Reciprocal excitatory and inhibitory relationships between thalamic and cortical responses appeared when neurons representing adjacent peripheral regions were studied. 6. The incidence of stimulus-induced inhibition of spontaneous activity in thalamus indicates the presence of topographically organized feedback connections responsible for suppressing activity in thalamic neurons that represent an area of skin surrounding the stimulated region. This provides evidence that inhibitory mechanisms shape the spatial response properties of neurons in the ventrobasal complex. 7. The results from latency and cross-correlation analyses collectively suggest that thalamocortical projections initiate activity primarily within granular layer IV. Subsequent activation of supragranular and infragranular cortical layers appears to proceed largely along parallel routes. The significance and limitations of neuronal efficacy measurements within the context of the somatosensory thalamocortical system are discussed further in the text.