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The Journal of Neuroscience, July 2, 2008, 28(27):6914-6925; doi:10.1523/JNEUROSCI.1660-08.2008

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Behavioral/Systems/Cognitive
Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Michael Pecka,^1,3 Antje Brand,² Oliver Behrend,² and Benedikt Grothe^1,2,3

¹Division of Neurobiology, Department Biology II, Ludwig-Maximilians University Munich, D-82152 Martinsried, Germany, ²Max Plank Institute of Neurobiology, D-82152 Martinsried, Germany, and ³Bernstein Center for Computational Neuroscience, D-81377 Munich, Germany

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

The dominant cue for localization of low-frequency sounds are microsecond differences in the time-of-arrival of sounds at the two ears [interaural time difference (ITD)]. In mammals, ITD sensitivity is established in the medial superior olive (MSO) by coincidence detection of excitatory inputs from both ears. Hence the relative delay of the binaural inputs is crucial for adjusting ITD sensitivity in MSO cells. How these delays are constructed is, however, still unknown. Specifically, the question of whether inhibitory inputs are involved in timing the net excitation in MSO cells, and if so how, is controversial. These inhibitory inputs derive from the nuclei of the trapezoid body, which have physiological and structural specializations for high-fidelity temporal transmission, raising the possibility that well timed inhibition is involved in tuning ITD sensitivity. Here, we present physiological and pharmacological data from in vivo extracellular MSO recordings in anesthetized gerbils. Reversible blockade of synaptic inhibition by iontophoretic application of the glycine antagonist strychnine increased firing rates and significantly shifted ITD sensitivity of MSO neurons. This indicates that glycinergic inhibition plays a major role in tuning the delays of binaural excitation. We also tonically applied glycine, which lowered firing rates but also shifted ITD sensitivity in a way analogous to strychnine. Hence tonic glycine application experimentally decoupled the effect of inhibition from the timing of its inputs. We conclude that, for proper ITD processing, not only is inhibition necessary, but it must also be precisely timed.

Key words: sound localization; pharmacology; strychnine; population coding; superior oliviary complex; brainstem

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Received Sept. 10, 2007; revised May 13, 2008; accepted May 23, 2008.

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

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