Self-regulation of adult thalamocortical neurons

J Neurophysiol. 2015 Jul;114(1):323-31. doi: 10.1152/jn.00800.2014. Epub 2015 May 6.

Abstract

The thalamus acts as a conduit for sensory and other information traveling to the cortex. In response to continuous sensory stimulation in vivo, the firing rate of thalamocortical neurons initially increases, but then within a minute firing rate decreases and T-type Ca(2+) channel-dependent action potential burst firing emerges. While neuromodulatory systems could play a role in this inhibitory response, we instead report a novel and cell-autonomous inhibitory mechanism intrinsic to the thalamic relay neuron. Direct intracellular stimulation of thalamocortical neuron firing initially triggered a continuous and high rate of action potential discharge, but within a minute membrane potential (Vm) was hyperpolarized and firing rate to the same stimulus was decreased. This self-inhibition was observed across a wide variety of thalamic nuclei, and in a subset firing mode switched from tonic to bursting. The self-inhibition resisted blockers of intracellular Ca(2+) signaling, Na(+)-K(+)-ATPases, and G protein-regulated inward rectifier (GIRK) channels as implicated in other neuron subtypes, but instead was in part inhibited by an ATP-sensitive K(+) channel blocker. The results identify a new homeostatic mechanism within the thalamus capable of gating excitatory signals at the single-cell level.

Keywords: KATP channel; excitability; thalamus.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Calcium / metabolism
  • Calcium Channels, T-Type / genetics
  • Calcium Channels, T-Type / metabolism
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / physiology*
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / metabolism
  • KATP Channels / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neural Pathways / drug effects
  • Neural Pathways / physiology
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology
  • Neurons / drug effects
  • Neurons / physiology*
  • Neurotransmitter Agents / pharmacology
  • Patch-Clamp Techniques
  • Potassium / metabolism
  • Sodium / metabolism
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Thalamus / drug effects
  • Thalamus / physiology*
  • Tissue Culture Techniques

Substances

  • Cacna1g protein, mouse
  • Calcium Channels, T-Type
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • KATP Channels
  • Neurotransmitter Agents
  • Sodium
  • Sodium-Potassium-Exchanging ATPase
  • Potassium
  • Calcium