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The Journal of Neuroscience, February 14, 2007, 27(7):1782-1790; doi:10.1523/JNEUROSCI.5335-06.2007

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Behavioral/Systems/Cognitive
Inhibiting the Inhibition: A Neuronal Network for Sound Localization in Reverberant Environments

Michael Pecka,^1 * Thomas P. Zahn,^1 * Bernadette Saunier-Rebori,^1 * Ida Siveke,¹ Felix Felmy,¹ Lutz Wiegrebe,¹ Achim Klug,¹ George D. Pollak,² and Benedikt Grothe¹

¹Division of Neurobiology, Department of Biology II, Ludwig-Maximilians-Universität Munich, D-82152 Martinsried, Germany, and ²Section of Neurobiology, The University of Texas at Austin, Austin, Texas 78712

Correspondence should be addressed to Prof. Dr. Benedikt Grothe, Department of Biology II, Biocenter, Ludwig-Maximilians-University of Munich, Grosshaderner Strasse 2, D-82152 Martinsried, Germany. Email: grothe{at}lmu.de

The precedence effect describes the phenomenon whereby echoes are spatially fused to the location of an initial sound by selectively suppressing the directional information of lagging sounds (echo suppression). Echo suppression is a prerequisite for faithful sound localization in natural environments but can break down depending on the behavioral context. To date, the neural mechanisms that suppress echo directional information without suppressing the perception of echoes themselves are not understood. We performed in vivo recordings in Mongolian gerbils of neurons of the dorsal nucleus of the lateral lemniscus (DNLL), a GABAergic brainstem nucleus that targets the auditory midbrain, and show that these DNLL neurons exhibit inhibition that persists tens of milliseconds beyond the stimulus offset, so-called persistent inhibition (PI). Using in vitro recordings, we demonstrate that PI stems from GABAergic projections from the opposite DNLL. Furthermore, these recordings show that PI is attributable to intrinsic features of this GABAergic innervation. Implementation of these physiological findings into a neuronal model of the auditory brainstem demonstrates that, on a circuit level, PI creates an enhancement of responsiveness to lagging sounds in auditory midbrain cells. Moreover, the model revealed that such response enhancement is a sufficient cue for an ideal observer to identify echoes and to exhibit echo suppression, which agrees closely with the percepts of human subjects.

Key words: echo suppression; precedence effect; Clifton effect; GABA; dorsal nucleus of the lateral lemniscus; inferior colliculus; binaural processing; modeling; persistent inhibition

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Received Sept. 7, 2006; revised Jan. 9, 2007; accepted Jan. 11, 2007.

Correspondence should be addressed to Prof. Dr. Benedikt Grothe, Department of Biology II, Biocenter, Ludwig-Maximilians-University of Munich, Grosshaderner Strasse 2, D-82152 Martinsried, Germany. Email: grothe{at}lmu.de

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				D. M. Caspary, L. Ling, J. G. Turner, and L. F. Hughes Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system J. Exp. Biol., June 1, 2008; 211(11): 1781 - 1791. [Abstract] [Full Text] [PDF]

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