Cellular mechanisms underlying intrathalamic augmenting responses of reticular and relay neurons

Augmenting (or incremental) responses are progressively growing potentials elicited by 5- to 15-Hz stimulation within the thalamus, cerebral cortex, or by setting into action reciprocal thalamocortical neuronal loops. These responses are associated with short-term plasticity processes in thalamic and cortical neurons. In the present study, in vivo intracellular recordings of thalamic reticular (RE) and thalamocortical (TC), as well as dual intracellular recordings, were used to explore the mechanisms of two types of intrathalamic augmenting responses elicited by thalamic stimuli at 10 Hz in decorticated cats. As recently described, after decortication, TC cells display incremental burst responses to thalamic stimuli that occur through either progressive depolarization (high threshold, HT) or progressive hyperpolarization leading to deinactivation of low-threshold (LT) spike bursts. Here, low-intensity stimuli (10 Hz) to dorsal thalamic nuclei elicited decremental responses in GABAergic RE cells, consisting of a progressive diminution in the number of action potentials in successive spike bursts, whereas higher stimulation (>50% of maximal strength) induced augmentation characterized by an increased number of spikes in repetitive responses. These opposing discharge patterns occurred in the absence of changes in the membrane potential of RE cells. In TC cells, augmentation depended on the thalamic site where testing volleys were applied. With stimuli applied closer to the site of impalement, augmenting resulted from a transformation from LT spike bursts into HT responses. Augmenting responses were followed by self-sustained oscillatory activity, within the frequency of spindles (7-14 Hz) or clock-like delta oscillation (1-4 Hz). As LT augmentation in TC cells results from their progressive hyperpolarization, we tested the effects exerted by the activating depolarizing system arising in the mesopontine cholinergic nuclei and found that such conditioning pulse-trains prevented the hyperpolarizing-rebound sequences as well as the LT augmenting in TC cells. We propose that the depolarization-dependent (HT) augmenting responses in TC cells result from decremental responses in RE neurons that are due to intra-RE inhibitory processes leading to disinhibition in target TC neurons, whereas LT-type augmenting in TC cells is produced mainly by incremental responses in GABAergic RE neurons.