Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states

Abstract

Spontaneous firing and antidromically or synaptically evoked discharges of 89 single neurons in centralis lateralis-paracentralis (CL-Pc) intralaminar thalamic nuclei were examined during waking and sleep states in behaving cats with chronic pontine lesions. Twenty-four neurons were activated synaptically at short latencies from the midbrain reticular formation (MRF) after anterograde degeneration of passing fibers. Sixty-five neurons were identified antidromically as projecting to motor or parietal association cortical areas; of them, 23 also could be excited synaptically from the MRF. These neurons were regarded as possibly being involved in the transfer toward the neocortex of the tonic excitation from the MRF during EEG-desynchronized behavioral states. Rates of spontaneous discharge in CL-Pc neurons doubled from synchronized sleep (S) to either wakefulness (W) or desynchronized sleep (D). First order measures of discharge patterns indicated that interval modes in both W and D states (greater than 10 msec) are significantly different from those in S (2.5 msec). During S, the intervals found in the less than 5-msec class indicated the intraburst frequencies; a later minor mode (200 to 350 msec) reflected the interburst silent periods. All neurons tested for antidromic activation from cortical areas had enhanced responsiveness in both W and D states as compared to S sleep. In some cases, the enhanced antidromic excitability was observed in conjunction with a transformation from initial segment spikes during S to full spikes in EEG-desynchronized states. During both W and D states, compared to S sleep, the probability of monosynaptically elicited single discharges to MRF stimulation was increased, and the latency and duration of high frequency bursts evoked by MRF volleys were shortened. We conclude that the features of cortically projecting intralaminar neurons that relay MRF activity fit in well with their hypothesized role in the tonic activation processes that characterize both W and D states. Several lines of evidence suggest that sustained hyperpolarization prevails in intralaminar neurons during S sleep. This is the basic prerequisite for thalamic bursting. The effect of long lasting inhibitory potentials in thalamic neurons provides a mechanism for closing sensory channels during S sleep.