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Differential regulation of GABA release and neuronal excitability mediated by neuropeptide Y₁ and Y₂ receptors in rat thalamic neurons

Qian-Quan Sun, Gustav Akk, John R. Huguenard and David A. Prince

1. Neuropeptide Y (NPY) produced inhibitory effects on neurons of the thalamic reticular nucleus (RT; n = 18) and adjacent ventral basal complex (VB; n = 22), which included hyperpolarization (~4 mV), a reduction in rebound and regular spikes and an increased membrane conductance. These effects were mediated predominantly via NPY₁ receptor activation of G-protein-activated, inwardly rectifying K⁺ (GIRK) channels.

2. NPY reduced the frequency of spontaneous GABA_A receptor-mediated inhibitory postsynaptic currents (sIPSCs) in RT (by 60 ± 7 %, n = 14) and VB neurons (by 25 ± 11 %, n = 16), but had no effect on the kinetic properties of sIPSCs. After removal of the RT nucleus, the inhibitory effects of NPY on sIPSCs in VB neurons remained (29 ± 7 %, n = 5). The synaptic effects were mediated via NPY₂ receptors.

3. NPY inhibited the frequency of miniature IPSCs (mIPSCs) in RT and VB neurons (by 63 ± 7 %, n = 5, and 37 ± 8 %, n = 10, respectively) in the presence of tetrodotoxin (TTX) (1 µM) but not TTX (1 µM) and Cd²⁺ (200 µM).

4. NPY inhibited evoked IPSCs in both RT (by 18 ± 3 %, n = 6) and VB (by 5 ± 4 %, n = 6) neurons without change in short-term synaptic plasticity.

5. We conclude that NPY₁ and NPY₂ receptors are functionally segregated in the thalamus: NPY₁ receptors are predominantly expressed at the somata and dendrites and directly reduce the excitability of neurons in both the RT and VB nuclei by activating GIRK channels. NPY₂ receptors are located at recurrent (RT) and feed-forward GABAergic terminals (VB) and downregulate GABA release via inhibition of Ca²⁺ influx from voltage-gated Ca²⁺ channels.

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