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 representat ions in the ventrobasal nucleus and primary somatosensory cortex of in tact, halothane-anesthetized rats. Thalamic and cortical neurons repre senting hairy skin on the forelimb were activated by hair movements pr oduced by a series of 50 or 100 discrete air jets. A corresponding set of neurons representing the glabrous pads of the hind paw were activa ted by a similar number of punctate mechanical displacements. 2. Corti cal electrode penetrations were histologically reconstructed, and 118 neurons in the glabrous skin representation exhibited cutaneous respon ses that were categorized into supragranular, granular, or infragranul ar groups according to their laminar position. Minimum latencies of co rtical 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 thes e groups suggests that stimulus-induced afferent activity reaches infr agranular and granular layers before contacting supragranular neurons. Average latencies were also calculated on responses occurring during the 1 st 20 trials, but the cortical distributions of these values ove rlapped considerably, and differences between the laminar groups were not statistically significant. 3. In several recording sites, two cort ical 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 loc ation is not the only determinant of response latency and that seriall y organized circuits are distributed within, as well as between, corti cal layers. 4. From a sample of 302 neurons exhibiting cutaneous respo nses 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 thalamocort ical interactions were found in 38 neuron pairs. Analysis of these sig nificant interactions revealed that thalamocortical connection strengt h, as measured by neuronal efficacy, was two to four times larger for neuron pairs having the cortical cell in granular layer IV than for ne uron pairs having an extragranular layer cortical neuron. There was no difference in thalamocortical connection strength between neuron pair s containing supra-or infragranular cortical neurons. 5. Summed perist imulus time histograms revealed stimulus-locked inhibition of spontane ous activity in 4% (8/195) of cortical and 18% (20/107) of thalamic ne urons. 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 ne uron's receptive field was stimulated. Reciprocal excitatory and inhib itory relationships between thalamic and cortical responses appeared w hen neurons representing adjacent peripheral regions were studied. 6. The incidence of stimulus-induced inhibition of spontaneous activity i n thalamus indicates the presence of topographically organized feedbac k connections responsible for suppressing activity in thalamic neurons that represent an area of skin surrounding the stimulated region. Thi s provides evidence that inhibitory mechanisms shape the spatial respo nse properties of neurons in the ventrobasal complex. 7. The results f rom latency and cross-correlation analyses collectively suggest that t halamocortical projections initiate activity primarily within granular layer IV. Subsequent activation of supragranular and infragranular co rtical layers appears to proceed largely along parallel routes. The si gnificance and limitations of neuronal efficacy measurements within th e context of the somatosensory thalamocortical system are discussed fu rther in the text.