GABAergic and glycinergic inhibition modulate monaural auditory response properties in the avian superior olivary nucleus

J Neurophysiol. 2011 May;105(5):2405-20. doi: 10.1152/jn.01088.2010. Epub 2011 Mar 2.

Abstract

The superior olivary nucleus (SON) is the primary source of inhibition in the avian auditory brainstem. While much is known about the role of inhibition at the SON's target nuclei, little is known about how the SON itself processes auditory information or how inhibition modulates these properties. Additionally, the synaptic physiology of inhibitory inputs within the SON has not been described. We investigated these questions using in vivo and in vitro electrophysiological techniques in combination with immunohistochemistry in the chicken, an organism for which the auditory brainstem has otherwise been well characterized. We provide a thorough characterization of monaural response properties in the SON and the influence of inhibitory input in shaping these features. We found that the SON contains a heterogeneous mixture of response patterns to acoustic stimulation and that in most neurons these responses are modulated by both GABAergic and glycinergic inhibitory inputs. Interestingly, many SON neurons tuned to low frequencies have robust phase-locking capability and the precision of this phase locking is enhanced by inhibitory inputs. On the synaptic level, we found that evoked and spontaneous inhibitory postsynaptic currents (IPSCs) within the SON are also mediated by both GABAergic and glycinergic inhibition in all neurons tested. Analysis of spontaneous IPSCs suggests that most SON cells receive a mixture of both purely GABAergic terminals, as well as terminals from which GABA and glycine are coreleased. Evidence for glycinergic signaling within the SON is a novel result that has important implications for understanding inhibitory function in the auditory brainstem.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation / methods
  • Animals
  • Animals, Newborn
  • Auditory Pathways / drug effects
  • Auditory Pathways / physiology*
  • Auditory Perception / drug effects
  • Auditory Perception / physiology*
  • Chickens
  • GABA Antagonists / pharmacology
  • Glycine / antagonists & inhibitors
  • Glycine / physiology
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / physiology
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Olivary Nucleus / drug effects
  • Olivary Nucleus / physiology*
  • Organ Culture Techniques
  • Receptors, GABA-A / physiology*
  • Receptors, Glycine / antagonists & inhibitors
  • Receptors, Glycine / physiology*
  • gamma-Aminobutyric Acid / physiology

Substances

  • GABA Antagonists
  • Receptors, GABA-A
  • Receptors, Glycine
  • gamma-Aminobutyric Acid
  • Glycine