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The Journal of Neuroscience, October 14, 2009, 29(41):13030-13041; doi:10.1523/JNEUROSCI.2477-09.2009

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Behavioral/Systems/Cognitive
Mechanisms Underlying Directional Selectivity for Frequency-Modulated Sweeps in the Inferior Colliculus Revealed by In Vivo Whole-Cell Recordings

Joshua X. Gittelman, Na Li, and George D. Pollak

Section of Neurobiology, Institute for Neuroscience, and Center for Perceptual Systems, The University of Texas at Austin, Austin, Texas 78712

Correspondence should be addressed to Joshua X. Gittelman, Section of Neurobiology, Institute for Neuroscience, and Center for Perceptual Systems, 337 Patterson Laboratories, The University of Texas at Austin, 1 University Station C0920, Austin, TX 78712. Email: jxg{at}mail.utexas.edu

Auditory neurons in the inferior colliculus (IC) show remarkable selectively in that they can distinguish between complex sounds that have identical spectral energy but different temporal structure, such as frequency modulations (FMs) that sweep either upward or downward. Extracellular recordings show that blocking inhibition locally reduces or eliminates response selectivity, suggesting that selectivity is created de novo in the IC, with inhibition playing a prominent role. However, these studies can only infer underlying mechanisms based on spike counts. Using in vivo whole-cell recordings, we examine the mechanisms underlying FM directional selectivity in the IC. We first report that spike threshold can strongly amplify directional selectivity in that the spike directionality was on average more than twice as large as the directionality of the postsynaptic potentials (PSPs). We then show that, in our sample of IC cells, PSP directional selectivity is not created de novo. Rather, we found that the preferred and null FMs evoked synaptic conductances of different magnitudes, indicating that the presynaptic neurons were directionally selective. Combining conductance data with modeling, we show that directionally dependent magnitude differences, not temporal differences, underlie PSP directionality. Modeling also shows that our results are consistent with extracellular studies in which blocking inhibition reduces or eliminates directionality. Our findings suggest that some IC cells use a rate code in their inputs rather than a time code and that highly selective discharge properties can be created by only minor adjustments in the synaptic strengths evoked by different signals.

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Received May 27, 2009; revised Aug. 13, 2009; accepted Sept. 5, 2009.

Correspondence should be addressed to Joshua X. Gittelman, Section of Neurobiology, Institute for Neuroscience, and Center for Perceptual Systems, 337 Patterson Laboratories, The University of Texas at Austin, 1 University Station C0920, Austin, TX 78712. Email: jxg{at}mail.utexas.edu

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