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Neural coding of sound envelope structure in songbirds

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Abstract

Songbirds are a well-established animal model to study the neural basis of learning, perception and production of complex vocalizations. In this system, telencephalic neurons in HVC present a state-dependent, highly selective response to auditory presentations of the bird’s own song (BOS). This property provides an opportunity to study the neural code behind a complex motor behavior. In this work, we explore whether changes in the temporal structure of the sound envelope can drive changes in the neural responses of highly selective HVC units. We generated an envelope-modified BOS (MOD) by reversing each syllable’s envelope but leaving the overall temporal structure of syllable spectra unchanged, which resulted in a subtle modification for each song syllable. We conducted in vivo electrophysiological recordings of HVC neurons in anaesthetized zebra finches (Taeniopygia guttata). Units analyzed presented a high BOS selectivity and lower response to MOD, but preserved the profile response shape. These results show that the temporal evolution of the sound envelope is being sensed by the avian song system and suggest that the biomechanical properties of the vocal apparatus could play a role in enhancing subtle sound differences.

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Abbreviations

BOS:

Bird’s own song

MOD:

Envelope-modified bird’s own song

REV:

Reverse song

CON:

Conspecific song

PSTH:

Post-stimulus Time Histogram

MAP:

Motif Activity Profile

MRA:

Mean Relative Amplitude

RRS:

Relative Response Strength

RRV:

Relative Response Variability

SC:

Spectral Centroid

IRR:

Spectral Irregularity

EMG:

Electromyography

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Acknowledgements

We thank Cecilia T. Herbert and Gabriel B. Mindlin for comments and discussions that greatly improved the manuscript. This work was partially supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina), Agencia Nacional de Promoción Científica y Tecnológica (ANCyT, Argentina), Universidad de Buenos Aires (UBA, Argentina) and National Institutes of Health (NIH, USA) through grant R01-DC-012859. Experimentation and surgical procedures were conducted following protocols approved by the Institutional Animal Care and Use Committee (IACUC) of the University of Buenos Aires.

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Authors and Affiliations

  1. Department of Physics, FCEN, University of Buenos Aires and IFIBA, CONICET, Intendente Guiraldes 2160, Pabellon 1, Ciudad Universitaria, Buenos Aires, 1428, Argentina

    Santiago Boari & Ana Amador

Authors
  1. Santiago Boari
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  2. Ana Amador
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Corresponding author

Correspondence to Ana Amador.

Electronic supplementary material

Below is the link to the electronic supplementary material.

359_2017_1238_MOESM1_ESM.pdf

Online Resource 2: MOD-to-BOS relative differences in spectral irregularity within each song syllable. In this figure, we show the temporal evolution of the spectral irregularity (IRR) as defined in the main text. Each subfigure (a-e) corresponds to the analysis for a different bird. IRR time traces are shown in the top panel, with black traces corresponding to BOS and red traces to MOD, respectively. The second panel shows the MOD-to-BOS relative difference in IRR, averaged over 5 ms windows. The two bottom panels show the BOS and MOD sound traces (arb. unit), color coded as above (sampling rate: 20 kHz). In the songs from all the birds present in our study, IRR is only slightly changed. Relative differences account for the similarity between the IRR of each syllable present in the BOS and MOD stimuli, as can be seen from the superimposing traces in each of the top panels in a-e and from the near-zero values for relative differences (second panel of a-e). Grouped data (f) shows a histogram for the relative difference values of the 22 syllables from the songs of the 5 birds present in this study (bin size = 0.005). From the 530 temporal bins analyzed, only a small percentage (2.8%) present a deviation larger than 3%. Distribution values are mostly within this range, and only a few rare cases present differences larger than 5% (0.4% of time bins). The small percentage of these occurrences and the fact that they are symmetrically distributed with respect to the peak at [-0.005,0.005] indicate that the induced changes in the creation of the MOD are subtle ones. Statistically, this distribution is indistinguishable from a zero-mean normal distribution (t-test, p=0.61). Comparable results are obtained for spectral centroid (see Online Resource 1) (PDF 2142 KB)

359_2017_1238_MOESM2_ESM.pdf

Online Resource 1: MOD-to-BOS relative differences in spectral centroid within each song syllable. In this figure, we show the temporal evolution of the spectral centroid (SC) as defined in the main text. Each subfigure (a-e) corresponds to the analysis for a different bird. SC time traces (in kHz) are shown in the top panel, with black traces corresponding to BOS and red traces to MOD, respectively. The second panel shows the MOD-to-BOS relative difference in SC, averaged over 5 ms windows. The two bottom panels show the BOS and MOD sound traces (arb. unit), color coded as above (sampling rate: 20 kHz). In the songs from all the birds present in our study, SC is only slightly changed. Relative differences account for the similarity between the SC of each syllable present in the BOS and MOD stimuli, as can be seen from the superimposing traces in each of the top panels in a-e and from the near-zero values for relative differences (second panel of a-e). Grouped data (f) shows a histogram for the relative difference values of the 22 syllables from the songs of the 5 birds present in this study (bin size = 0.005). From the 530 temporal bins analyzed, only a small percentage (2%) present a deviation larger than 3%. Distribution values are mostly within this range, and only a few rare cases present differences larger than 5% (0.2% of time bins). The small percentage of these occurrences and the fact that they are symmetrically distributed with respect to the peak at [-0.005,0.005] indicate that the induced changes in the creation of the MOD are subtle ones. Statistically, this distribution is indistinguishable from a zero-mean normal distribution (t-test, p=0.17). Comparable results are obtained for spectral irregularity (see Online Resource 2) (PDF 2152 KB)

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Boari, S., Amador, A. Neural coding of sound envelope structure in songbirds. J Comp Physiol A 204, 285–294 (2018). https://doi.org/10.1007/s00359-017-1238-9

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