Feedforward inhibitory control of sensory information in higher-order thalamic nuclei

Philippe Lavallée, Nadia Urbain, Caroline Dufresne, Hajnalka Bokor, L. Acsády, Martin Deschênes

Research output: Contribution to journalArticle

98 Citations (Scopus)

Abstract

Sensory stimuli evoke strong responses in thalamic relay cells, which ensure a faithful relay of information to the neocortex. However, relay cells of the posterior thalamic nuclear group in rodents, despite receiving significant trigeminal input, respond poorly to vibrissa deflection. Here we show that sensory transmission in this nucleus is impeded by fast feedforward inhibition mediated by GABAergic neurons of the zona incerta. Intracellular recordings of posterior group neurons revealed that the first synaptic event after whisker deflection is a prominent inhibition. Whisker-evoked EPSPs with fast rise time and longer onset latency are unveiled only after lesioning the zona incerta. Excitation survives barrel cortex lesion, demonstrating its peripheral origin. Electron microscopic data confirm that trigeminal axons make large synaptic terminals on the proximal dendrites of posterior group cells and on the somata of incertal neurons. Thus, the connectivity of the system allows an unusual situation in which inhibition precedes ascending excitation resulting in efficient shunting of the responses. The dominance of inhibition over excitation strongly suggests that the paralemniscal pathway is not designed to relay inputs triggered by passive whisker deflection. Instead, we propose that this pathway operates through disinhibition, and that the posterior group forwards to the cerebral cortex sensory information that is contingent on motor instructions.

Original languageEnglish
Pages (from-to)7489-7498
Number of pages10
JournalJournal of Neuroscience
Volume25
Issue number33
DOIs
Publication statusPublished - Aug 17 2005

Fingerprint

Vibrissae
Thalamic Nuclei
Posterior Thalamic Nuclei
Neurons
GABAergic Neurons
Excitatory Postsynaptic Potentials
Neocortex
Presynaptic Terminals
Carisoprodol
Dendrites
Cerebral Cortex
Axons
Rodentia
Electrons
Zona Incerta

Keywords

  • Barrel
  • Inhibition
  • Thalamus
  • Trigeminal
  • Vibrissa
  • Whisker
  • Zona incerta

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Feedforward inhibitory control of sensory information in higher-order thalamic nuclei. / Lavallée, Philippe; Urbain, Nadia; Dufresne, Caroline; Bokor, Hajnalka; Acsády, L.; Deschênes, Martin.

In: Journal of Neuroscience, Vol. 25, No. 33, 17.08.2005, p. 7489-7498.

Research output: Contribution to journalArticle

Lavallée, Philippe ; Urbain, Nadia ; Dufresne, Caroline ; Bokor, Hajnalka ; Acsády, L. ; Deschênes, Martin. / Feedforward inhibitory control of sensory information in higher-order thalamic nuclei. In: Journal of Neuroscience. 2005 ; Vol. 25, No. 33. pp. 7489-7498.
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