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The Journal of Neuroscience, July 29, 2009, 29(30):9625-9634; doi:10.1523/JNEUROSCI.0103-09.2009

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Behavioral/Systems/Cognitive
Heterogeneous Kinetics and Pharmacology of Synaptic Inhibition in the Chick Auditory Brainstem

Sidney P. Kuo, Laura A. Bradley, and Laurence O. Trussell

Oregon Hearing Research Center and Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239

Correspondence should be addressed to Sidney P. Kuo, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L335A, Portland, OR 97239. Email: kuos{at}ohsu.edu

Identification of shared features between avian and mammalian auditory brainstem circuits has provided much insight into the mechanisms underlying early auditory processing. However, previous studies have highlighted an apparent difference in inhibitory systems; synaptic inhibition is thought to be slow and GABAergic in birds but to have fast kinetics and be predominantly glycinergic in mammals. Using patch-clamp recordings in chick brainstem slices, we found that this distinction is not exclusively true. Consistent with previous work, IPSCs in nucleus magnocellularis (NM) were slow and mediated by GABAA receptors. However, IPSCs in nucleus laminaris (NL) and a subset of neurons in nucleus angularis (NA) had rapid time courses twofold to threefold faster than those in NM. Furthermore, we found that IPSCs in NA were mediated by both glycine and GABAA receptors, demonstrating for the first time a role for fast glycinergic transmission in the avian auditory brainstem. Although NM, NL, and NA have unique roles in auditory processing, the majority of inhibitory input to each nucleus arises from the same source, ipsilateral superior olivary nucleus (SON). Our results demonstrate remarkable diversity of inhibitory transmission among the avian brainstem nuclei and suggest that differential glycine and GABAA receptor activity tailors inhibition to the specific functional roles of NM, NL, and NA despite common SON input. We additionally observed that glycinergic/GABAergic activity in NA was usually depolarizing and could elicit spiking activity in NA neurons. Because NA projects to SON, these excitatory effects may influence the recruitment of inhibitory activity in the brainstem nuclei.

Received Jan. 7, 2009; revised June 9, 2009; accepted June 24, 2009.

Correspondence should be addressed to Sidney P. Kuo, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L335A, Portland, OR 97239. Email: kuos{at}ohsu.edu






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