CROSS-CORRELATION ANALYSIS OF CUNEOTHALAMIC INTERACTIONS IN THE RAT SOMATOSENSORY SYSTEM - INFLUENCE OF RECEPTIVE-FIELD TOPOGRAPHY AND COMPARISONS WITH THALAMOCORTICAL INTERACTIONS

1. We simultaneously recorded neuronal responses to cutaneous stimulat ion from matched somatotopic representations in the nucleus cuneatus a nd ventrobasal complex of intact, halothane-anesthetized rats. A total of 95 cuneate and 86 thalamic neurons representing hairy skin on the forelimb were activated by hair movements produced by air jets at mult iple skin sites. Mean responsiveness was higher among neurons in nucle us cuneatus (34.4 spikes per stimulus) than in thalamus(23.7 spikes pe r stimulus), a result that was consistent with the greater proportion of ''sustained'' responses recorded in nucleus cuneatus(80% ) than in the thalamus (62%). 2. Cross-correlation analysis of 166 pairs of cune ate and thalamic neurons showed that 56 neuron pairs displayed time-lo cked correlations in activity that were characterized primarily by exc itatory interactions (44 pairs) or a combination of excitatory and inh ibitory interactions (10 pairs). Unilateral interactions in the cuneot halamic direction (31 pairs) and reverse direction (11 pairs) were obs erved, as well as muItiphasic interactions in both directions(14 pairs ). Most excitatory interactions involved intervals of 1-7 ms between s uccessive cuneate and thalamic discharges, whereas most inhibitory inf luences involved intervals >7 ms. Connection strength, defined by the ratio of time-linked interactions to the number of cuneate discharges, varied widely among neuron pairs but was largest for interactions inv olving interspike intervals of less than or equal to 15 ms. 3. The rel ationship between connection strength and receptive field topography w as analyzed in 103 cuneate-thalamic neuron pairs. The region of skin s hared by both neurons varied substantially among neuron pairs and the probability of detecting interactions increased proportionately with l arger amounts of receptive field overlap. Neuron pairs with moderate ( 25-50%) amounts of receptive field overlap had connection strengths 3- 4 times greater than neuron pairs with minimal (0-25%) overlap. Connec tion strength was essentially identical, however, for neuron pairs wit h moderate or large (>50%) amounts of overlap. 4. Cuneate-thalamic neu ron pairs displaying functional connections were usually tested at mul tiple peripheral sites, but only 37% (18 of 49) of these neuron pairs displayed interactions at more than one stimulation site. Stimulation at different sites altered the timing of interactions in seven neuron pairs, including three that showed timing shifts across time zero in t he cross-correlation histogram. In neuron pairs displaying interaction s at multiple sites, connection strengths for 67% of the cases were st rongest when stimulation was delivered within the region of receptive field overlap. Among 31 neuron pairs displaying interactions at a sing le stimulation site, 57% of these sites were in the central region of overlap. 5. In 10 experiments we tested thalamic responsiveness before and after making a discrete electrolytic microlesion at the cuneate r ecording site. In most cases thalamic neurons became less responsive a nd the decrease in activity was proportional to the maximum connection strength associated with each pair of recording sites. 6. We compared cuneate-thalamic interactions with thalamic-cortical interactions obt ained from a previous study using identical protocols. Stimulus-induce d responses were largest in nucleus cuneatus and were progressively sm aller in the somatosensory thalamus and cortex. Analysis of the tempor al structure of the crosscorrelation histograms revealed that cuneotha lamic interactions had less variability and involved shorter temporal intervals than thalamocortical interactions. These differences were co nsistent with evidence suggesting that cuneate-thalamic interactions a re more likely to involve monosynaptic connections. 7. Cuneate-thalami c and thalamic-cortical interactions were analyzed during spontaneous and stimulus-induced activity. Interactions between thalamic and corti cal neurons were equally likely during spontaneous or stimulus-induced activity, whereas cuneate-thalamic interactions occurred almost exclu sively during stimulus-induced activity. These results showed that cun eothalamic and thalamocortical projections are differentially involved in relaying sensory or state-dependent information. Analysis of stimu lus-induced interactions suggests that cuneothalamic synaptic connecti ons are more efficacious than thalamocortical synapses. These results are consonant with known anatomic differences between cuneothalamic an d thalamocortical connections and are discussed in the text.