Short-lasting nicotinic and long-lasting muscarinic depolarizing responses of thalamocortical neurons to stimulation of mesopontine cholinergic nuclei

R. C. Dossi, D. Pare, M. Steriade

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The responses of thalamocortical neurons to stimulation of mesopontine [peribrachial (PB) and laterodorsal (LDT)] cholinergic nuclei were studied intracellularly in urethan-anesthetized cats. Neurons recorded from anterior thalamic (AT), ventroanterior-ventrolateral (VA-VL) and rostral intralaminar centrolateral (CL) nuclei were physiologically identified by their orthodromic responses to prethalamic stimulation and/or antidromic activation from the cerebral cortex. Besides early excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) that were not sensitive to cholinergic antagonists, two types of cholinergic responses were elicited by PB/LDT stimulation: a short-lasting and a late, long-lasting depolarization. All these components survived monoamine depletion by reserpine. The latency of the short-lasting depolarizing response was 147.4 ± 27.3 (SE) ms. The response lasted for 1.3 ± 0.1 s and had a peak amplitude of 4.2 ± 0.3 mV. This component was associated with 10-30% increase in membrane conductance and was abolished by systemic administration of the nicotinic antagonist mecamylamine. The long-lasting depolarizing response had a latency of 1.2 ± 0.1 s, a duration of 20.8 ± 2.2 s, and a peak amplitude of 5.4 ± 0.4 mV. Similar values were found in decorticated animals. The duration and amplitude of the late depolarizing component were dependent on stimulation parameters and membrane potential. This response increased under depolarizing current, decreased and eventually disappeared under hyperpolarizing current, and was associated on average with 40% increase in apparent input resistance. After systemic administration of the muscarinic antagonist scopolamine, the long-lasting depolarization disappeared; the surviving short-lasting depolarization was subsequently abolished by mecamylamine. The prolonged depolarizing response of thalamocortical neurons to mesopontine cholinergic stimulation was accompanied by a desynchronization of the electroencephalogram (EEG). These two phenomena had a similar time course. Stimulation of deep cerebellar nuclei, whose axons traverse the PB area, did not induce a long-lasting depolarization of target thalamic cells, nor an EEG desynchronization. These data demonstrate that, in addition to an initial nicotinic excitation, brain stem cholinergic stimulation elicits a late, long-lasting muscarinic depolarization of thalamocortical neurons. We suggest that the prolonged depolarization plays an important role in cortical activation.

Original languageEnglish (US)
Pages (from-to)393-406
Number of pages14
JournalJournal of neurophysiology
Issue number3
StatePublished - 1991
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology


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