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Excitatory Actions of Vasoactive Intestinal Peptide on Mouse Thalamocortical Neurons Are Mediated by VPAC₂ Receptors

Department of Molecular and Integrative Physiology, University of Illinois; Department of Pharmacology, College of Medicine, University of Illinois; and Beckman Institute, University of Illinois, Urbana-Champaign, Urbana, Illinois

Submitted 21 October 2005; accepted in final form 17 April 2006

Thalamic nuclei can generate intrathalamic rhythms similar to those observed at various arousal levels and pathophysiological conditions such as absence epilepsy. These rhythmic activities can be altered by a variety of neuromodulators that arise from brain stem regions as well as those that are intrinsic to the thalamic circuitry. Vasoactive intestinal peptide (VIP) is a neuropeptide localized within the thalamus and strongly attenuates intrathalamic rhythms via an unidentified receptor subtype. We have used transgenic mice lacking a specific VIP receptor, VPAC₂, to identify its role in VIP-mediated actions in the thalamus. VIP strongly attenuated both the slow, 2–4 Hz and spindle-like 5–8 Hz rhythmic activities in slices from wild-type mice (VPAC₂^+/+) but not in slices from VPAC₂ receptor knock-out mice (VPAC₂^–/–), which suggests a major role of VPAC₂ receptors in the antioscillatory actions of VIP. Intracellular recordings revealed that VIP depolarized all relay neurons tested from VPAC₂^+/+ mice. In VPAC₂^–/– mice, however, VIP produced no membrane depolarization in 80% of neurons tested. In relay neurons from VPAC₂+/+ mice, VIP enhanced the hyperpolarization-activated mixed cation current, I_h, via cyclic AMP activity, but VIP did not alter I_h in VPAC₂–/– mice. In VPAC₂–/– mice, pituitary adenylate cyclase activating-polypeptide (PACAP) depolarized the majority of relay neurons via I_h enhancement presumably via PAC₁ receptor activation. Our findings suggest that VIP-mediated actions are predominantly mediated by VPAC₂ receptors, but PAC₁ receptors may play a minor role. The excitatory actions of VIP and PACAP suggest these peptides may not only regulate intrathalamic rhythmic activities, but also may influence information transfer through thalamocortical circuits.

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