Tonotopic Specializations in Number, Size, and Reversal Potential of GABAergic Inputs Fine-Tune Temporal Coding at Avian Cochlear Nucleus

Abstract

GABAergic inhibition in neurons plays a critical role in determining the output of neural circuits. Neurons in avian nucleus magnocellularis (NM) use several tonotopic-region-dependent specializations to relay the timing information of sound in the auditory nerve to higher auditory nuclei. Previously, we showed that feedforward GABAergic inhibition in NM has a different dependence on the level of auditory nerve activity, with the low-frequency region having a low-threshold and linear relationship, while the high-frequency region has a high-threshold and step-like relationship. However, it remains unclear how the GABAergic synapses are tonotopically regulated and interact with other specializations of NM neurons. In this study, we examined GABAergic transmission in the NM of chickens of both sexes and explored its contributions to the temporal coding of sound at each tonotopic region. We found that the number and size of unitary GABAergic currents and their reversal potential were finely tuned at each tonotopic region in the NM. At the lower-frequency region, unitary GABAergic currents were larger in number but smaller in size. In addition, their reversal potential was close to the resting potential of neurons, which enabled reliable inhibition despite the smaller potassium conductance. At the higher-frequency region, on the other hand, unitary GABAergic currents were fewer, larger, and highly depolarizing, which enabled powerful inhibition via activating the large potassium conductance. Thus, we propose that GABAergic synapses are coordinated with the characteristics of excitatory synapses and postsynaptic neurons, ensuring the temporal coding for wide frequency and intensity ranges.

SIGNIFICANCE STATEMENT We found in avian cochlear nucleus that the number and size of unitary GABAergic inputs differed among tonotopic regions and correlated to respective excitatory inputs; it was larger in number but smaller in size for neurons tuned to lower-frequency sound. Furthermore, GABAergic reversal potential also differed among the regions in accordance with the size of Kv1 current; it was less depolarized in the lower-frequency neurons with smaller Kv1 current. These differentiations of GABAergic transmission maximized the effects of inhibition at each tonotopic region, ensuring precise and reliable temporal coding across frequencies and intensities. Our results emphasize the importance of optimizing characteristics of GABAergic transmission within individual neurons for proper neural circuit function.