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The Journal of Neuroscience, August 17, 2005, 25(33):7489-7498; doi:10.1523/JNEUROSCI.2301-05.2005

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Behavioral/Systems/Cognitive
Feedforward Inhibitory Control of Sensory Information in Higher-Order Thalamic Nuclei

Philippe Lavallée,¹ Nadia Urbain,¹ Caroline Dufresne,¹ Hajnalka Bokor,² László Acsády,² and Martin Deschênes¹

¹Centre de Recherche Université Laval Robert-Giffard, Hôpital Robert-Giffard, Québec, Canada G1J 2G3, and ²Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest H-1450, Hungary

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.

Key words: barrel; inhibition; thalamus; trigeminal; vibrissa; whisker; zona incerta

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Received April 28, 2005; revised July 4, 2005; accepted July 6, 2005.

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