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The Journal of Neuroscience, January 2, 2008, 28(1):80-90; doi:10.1523/JNEUROSCI.3572-07.2008

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Behavioral/Systems/Cognitive
Glycinergic "Inhibition" Mediates Selective Excitatory Responses to Combinations of Sounds

Jason Tait Sanchez,^1,2 Donald Gans,^1,2 and Jeffrey J. Wenstrup¹

¹Department of Neurobiology, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272, and ²School of Speech Pathology and Audiology, Kent State University, Kent, Ohio 44270

Correspondence should be addressed to Jeffrey J. Wenstrup, Department of Neurobiology, Northeastern Ohio Universities College of Medicine, 4209 State Route 44, P.O. Box 95, Rootstown, OH 44272. Email: jjw{at}neoucom.edu

In the mustached bat's inferior colliculus (IC), combination-sensitive neurons display time-sensitive facilitatory interactions between inputs tuned to distinct spectral elements in sonar or social vocalizations. Here we compare roles of ionotropic receptors to glutamate (iGluRs), glycine (GlyRs), and GABA (GABA_ARs) in facilitatory combination-sensitive interactions. Facilitatory responses to 36 single IC neurons were recorded before, during, and after local application of antagonists to these receptors. The NMDA receptor antagonist CPP [(±)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid], alone (n = 14) or combined with AMPA receptor antagonist NBQX (n = 22), significantly reduced or eliminated responses to best frequency (BF) sounds across a broad range of sound levels, but did not eliminate combination-sensitive facilitation. In a subset of neurons, GABA_AR blockers bicuculline or gabazine were applied in addition to iGluR blockers. GABA_AR blockers did not "uncover" residual iGluR-mediated excitation, and only rarely eliminated facilitation. In nearly all neurons for which the GlyR antagonist strychnine was applied in addition to iGluR blockade (22 of 23 neurons, with or without GABA_AR blockade), facilitatory interactions were eliminated. Thus, neither glutamate nor GABA neurotransmission are required for facilitatory combination-sensitive interactions in IC. Instead, facilitation may depend entirely on glycinergic inputs that are presumed to be inhibitory. We propose that glycinergic inputs tuned to two distinct spectral elements in vocal signals each activate postinhibitory rebound excitation. When rebound excitations from two spectral elements coincide, the neuron discharges. Excitation from glutamatergic inputs, tuned to the BF of the neuron, is superimposed onto this facilitatory interaction, presumably mediating responses to a broader range of acoustic signals.

Key words: AMPA; combination sensitivity; glutamate; inferior colliculus; mustached bat; NMDA

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Received Aug. 6, 2007; revised Oct. 30, 2007; accepted Nov. 4, 2007.

Correspondence should be addressed to Jeffrey J. Wenstrup, Department of Neurobiology, Northeastern Ohio Universities College of Medicine, 4209 State Route 44, P.O. Box 95, Rootstown, OH 44272. Email: jjw{at}neoucom.edu

This article has been cited by other articles:

				L. M. Hurley, J. A. Tracy, and A. Bohorquez Serotonin 1B Receptor Modulates Frequency Response Curves and Spectral Integration in the Inferior Colliculus by Reducing GABAergic Inhibition J Neurophysiol, September 1, 2008; 100(3): 1656 - 1667. [Abstract] [Full Text] [PDF]

				D. C. Peterson, S. Voytenko, D. Gans, A. Galazyuk, and J. Wenstrup Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus J Neurophysiol, August 1, 2008; 100(2): 629 - 645. [Abstract] [Full Text] [PDF]

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