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Research ArticleNew Research, Sensory and Motor Systems

Synaptic Inhibition in Avian Interaural Level Difference Sound Localizing Neurons

Rebecca J. Curry and Yong Lu
eNeuro 9 December 2016, 3 (6) ENEURO.0309-16.2016; DOI: https://doi.org/10.1523/ENEURO.0309-16.2016
Rebecca J. Curry
1Department of Anatomy and Neurobiology, College of Medicine, Northeast Ohio Medical University, Rootstown, Ohio 44272
2School of Biomedical Sciences, Kent State University, Kent, Ohio 44240
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Yong Lu
1Department of Anatomy and Neurobiology, College of Medicine, Northeast Ohio Medical University, Rootstown, Ohio 44272
2School of Biomedical Sciences, Kent State University, Kent, Ohio 44240
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Abstract

Synaptic inhibition plays a fundamental role in the neural computation of the interaural level difference (ILD), an important cue for the localization of high-frequency sound. Here, we studied the inhibitory synaptic currents in the chicken posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp), the first binaural level difference encoder of the avian auditory pathway. Using whole-cell recordings in brain slices, we provide the first evidence confirming a monosynaptic inhibition driven by direct electrical and chemical stimulation of the contralateral LLDp, establishing the reciprocal inhibitory connection between the two LLDps, a long-standing assumption in the field. This inhibition was largely mediated by GABAA receptors; however, functional glycine receptors were also identified. The reversal potential for the Cl− channels measured with gramicidin-perforated patch recordings was hyperpolarizing (−88 mV), corresponding to a low intracellular Cl− concentration (5.2 mm). Pharmacological manipulations of KCC2 (outwardly Cl− transporter) activity demonstrate that LLDp neurons can maintain a low intracellular Cl− concentration under a high Cl− load, allowing for the maintenance of hyperpolarizing inhibition. We further demonstrate that hyperpolarizing inhibition was more effective at regulating cellular excitability than depolarizing inhibition in LLDp neurons.

  • dorsal nucleus of the lateral lemniscus
  • GABAA receptor
  • interaural level difference
  • reversal potential
  • synaptic inhibition

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by Department of Health and Human Services/National Institutes of Health/National Institute on Deafness and other Communication Disorders Grants F31-DC-015707 (to R.J.C.) and R01-DC-008984 (Y.L.), and an Institutional Bridge Fund grant (Y.L.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 3 (6)
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Vol. 3, Issue 6
November/December 2016
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Synaptic Inhibition in Avian Interaural Level Difference Sound Localizing Neurons
Rebecca J. Curry, Yong Lu
eNeuro 9 December 2016, 3 (6) ENEURO.0309-16.2016; DOI: 10.1523/ENEURO.0309-16.2016

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Synaptic Inhibition in Avian Interaural Level Difference Sound Localizing Neurons
Rebecca J. Curry, Yong Lu
eNeuro 9 December 2016, 3 (6) ENEURO.0309-16.2016; DOI: 10.1523/ENEURO.0309-16.2016
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Keywords

  • dorsal nucleus of the lateral lemniscus
  • GABAA receptor
  • interaural level difference
  • reversal potential
  • synaptic inhibition

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