Two GABA A responses with distinct kinetics in a sound localization circuit

Abstract

The temporal characteristics and functional diversity of GABAergic inhibition are determined by the spatiotemporal neurotransmitter profile, intrinsic properties of GABA A receptors, and other factors. Here, we report two distinct GABA A responses and the underlying mechanisms in neurons of the chicken nucleus laminaris (NL), the first encoder of interaural time difference for sound localization in birds. The time course of the postsynaptic GABA A currents in NL neurons, recorded with whole-cell voltage clamp, differed between different characteristic frequency (CF) regions. Compared to low-CF (LF) neurons, middle/high-CF (MF/HF) neurons had significantly slower IPSCs, with a 2.6-fold difference in the decay time constants of spontaneous IPSCs and a 5.3-fold difference in the decay of IPSCs elicited by single-pulse stimulus. Such differences were especially dramatic when IPSCs were elicited by train stimulations at physiologically relevant frequencies, and at high stimulus intensities. To account for these distinct GABA A responses, we showed that MF/HF neurons exhibited more prominent asynchronous release of GABA. Supporting this observation, replacement of extracellular Ca 2+ with Sr 2+ increased the decay of IPSCs in LF neurons, and EGTA-AM reduced the decay of IPSCs in MF/HF neurons. Furthermore, pharmacological evidence suggests that GABA spillover plays a greater role in prolonging the IPSCs of MF/HF neurons. Consequently, under whole-cell current clamp, synaptically released GABA produced short- and long-lasting suppression of the neuronal excitability of LF and MF/HF neurons, respectively. Taken together, these results suggest that the GABAergic inputs to NL neurons may exert a dynamic modulation of interaural time difference (ITD) coding in a CF-dependent manner. © 2012 The Authors. The Journal of Physiology © 2012 The Physiological Society.