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Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds

Abstract

Vocal communicators discriminate conspecific vocalizations from other sounds and recognize the vocalizations of individuals. To identify neural mechanisms for the discrimination of such natural sounds, we compared the linear spectro-temporal tuning properties of auditory midbrain and forebrain neurons in zebra finches with the statistics of natural sounds, including song. Here, we demonstrate that ensembles of auditory neurons are tuned to auditory features that enhance the acoustic differences between classes of natural sounds, and among the songs of individual birds. Tuning specifically avoids the spectro-temporal modulations that are redundant across natural sounds and therefore provide little information; rather, it overlaps with the temporal modulations that differ most across sounds. By comparing the real tuning and a less selective model of spectro-temporal tuning, we found that the real modulation tuning increases the neural discrimination of different sounds. Additionally, auditory neurons discriminate among zebra finch song segments better than among synthetic sound segments.

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Figure 1: Spectro-temporal modulations in song and modulation-limited (ml) noise.
Figure 2: Recording sites and analysis of neural tuning.
Figure 3: Selective ensemble modulation tuning.
Figure 4: Tuning efficiency in response to modulation-limited noise.
Figure 5: Natural versus model modulation tuning and the neural discrimination of natural sounds.
Figure 6: Neural discrimination of natural versus synthetic sounds.

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Acknowledgements

We thank P. Gill for discussion and assistance in the data analysis. We thank J. Mazer for insightful comments on an earlier version of this manuscript. This work was supported by US National Institute of Deafness and Communication Disorders grants to S.M.N.W. and F.E.T. and US National Institute of Mental Health grants to F.E.T. and T.E.F.

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Correspondence to Sarah M N Woolley.

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Supplementary information

Supplementary Fig. 1

Contribution of the non-linear response to the neurogram distance. (PDF 152 kb)

Supplementary Fig. 2

Correlation between spectrogram distance and neurogram distance. (PDF 154 kb)

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Woolley, S., Fremouw, T., Hsu, A. et al. Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8, 1371–1379 (2005). https://doi.org/10.1038/nn1536

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