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The Journal of Neuroscience, May 2, 2007, 27(18):4882-4893; doi:10.1523/JNEUROSCI.4342-06.2007

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Behavioral/Systems/Cognitive
Spectrotemporal Receptive Fields in the Inferior Colliculus Revealing Selectivity for Spectral Motion in Conspecific Vocalizations

Sari Andoni, 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 George D. Pollak, Section of Neurobiology, Institute for Neuroscience, and Center for Perceptual Systems, The University of Texas at Austin, Austin, TX 78712. Email: gpollak{at}mail.utexas.edu

Frequency modulations are a prominent feature of animal vocalizations and human speech. Here we investigated how neurons in the inferior colliculus (IC) of Mexican free-tailed bats respond to the frequency-modulated (FM) direction and velocity of complex signals by extracting their spectrotemporal receptive fields (STRFs) using a family of upward- and downward-moving ripple stimuli. STRFs were obtained in more than half of the cells that were sampled. To verify the validity of each STRF, we compared their features both with tone-evoked responses and by convolving the STRF with several conspecific calls. We show that responses to tones are in close agreement with the STRF and that the responses predicted by convolutions compare favorably with responses evoked by those calls. The high predictability showed that the STRF captured most of the excitatory and inhibitory properties of IC cells. Most neurons were selective for the direction and velocity of spectral motion with a majority favoring the downward FM direction, and most had spectrum–time inseparability that correlated with their direction selectivity. Furthermore, blocking inhibition significantly reduced the directional selectivity of these neurons, suggesting that inhibition shapes FM direction selectivity in the IC. Finally, we decomposed the natural calls into their ripple components and show that most species-specific calls have downward-sweeping FM components with sweep velocities that correspond with the preferred sweep velocities of IC neurons. This close quantitative correspondence among features of signals and responses suggests that IC cells are tuned by inhibition to respond optimally to spectral motion cues present in their conspecific vocalizations.

Key words: spectrotemporal receptive field; inferior colliculus; conspecific calls; inhibition; inseparability; direction selectivity; velocity tuning; FM sweep

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Received Oct. 4, 2006; revised March 27, 2007; accepted March 28, 2007.

Correspondence should be addressed to George D. Pollak, Section of Neurobiology, Institute for Neuroscience, and Center for Perceptual Systems, The University of Texas at Austin, Austin, TX 78712. Email: gpollak{at}mail.utexas.edu

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