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Nonlinear processing of a multicomponent communication signal by combination-sensitive neurons in the anuran inferior colliculus

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Abstract

Diverse animals communicate using multicomponent signals. How a receiver’s central nervous system integrates multiple signal components remains largely unknown. We investigated how female green treefrogs (Hyla cinerea) integrate the multiple spectral components present in male advertisement calls. Typical calls have a bimodal spectrum consisting of formant-like low-frequency (~0.9 kHz) and high-frequency (~2.7 kHz) components that are transduced by different sensory organs in the inner ear. In behavioral experiments, only bimodal calls reliably elicited phonotaxis in no-choice tests, and they were selectively chosen over unimodal calls in two-alternative choice tests. Single neurons in the inferior colliculus of awake, passively listening subjects were classified as combination-insensitive units (27.9%) or combination-sensitive units (72.1%) based on patterns of relative responses to the same bimodal and unimodal calls. Combination-insensitive units responded similarly to the bimodal call and one or both unimodal calls. In contrast, combination-sensitive units exhibited both linear responses (i.e., linear summation) and, more commonly, nonlinear responses (e.g., facilitation, compressive summation, or suppression) to the spectral combination in the bimodal call. These results are consistent with the hypothesis that nonlinearities play potentially critical roles in spectral integration and in the neural processing of multicomponent communication signals.

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Notes

  1. Averaging upper and lower bounds differing by 2.5 dB on a linear scale yields threshold estimates that are 0.1775 dB higher than those averaged on a dB scale.

  2. Note that our definition of MTR units differs from the use of this designation by Fuzessery and Feng (1982, 1983), who used it to refer to units that exhibited facilitated responses to combinations of multiple tones.

Abbreviations

ANOVA:

Analysis of variance

BEF:

Best excitatory frequency

CV:

Coefficient of variation

DFA:

Discriminant function analysis

FTC:

Frequency tuning curve

GABA:

Gamma-aminobutyric acid

IC:

Inferior colliculus

MTR:

Multi-tone responder

SD:

Standard deviation

SPL:

Sound pressure level

STR:

Single-tone responder

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Acknowledgements

All experimental procedures were approved by the University of Minnesota Institutional Animal Care and Use Committee (1103A97192, 1401-31258A). The authors thank Peter Narins for his invitation to contribute to this Special Issue; Christopher Maldonado and Gary Calkins for access to frogs in Texas; Jim Hall for advice on marking recording sites; Camille Herteaux, Mary Elson, and Adam Hartman for animal care; two anonymous reviewers for helpful feedback on an earlier version of the manuscript; and the National Science Foundation for a grant to MAB (NSF IOS-1452831) in support of this research.

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Author notes

  1. Norman Lee

    Present address: Biology Department, St. Olaf College, Northfield, MN, 55057, USA

  2. Katrina M. Schrode

    Present address: Department of Otolaryngology, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA

Authors and Affiliations

  1. Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, 55108, USA

    Norman Lee & Mark A. Bee

  2. Graduate Program in Neuroscience, University of Minnesota, Minneapolis, MN, 55455, USA

    Katrina M. Schrode & Mark A. Bee

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  1. Norman Lee
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Correspondence to Mark A. Bee.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

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Lee, N., Schrode, K.M. & Bee, M.A. Nonlinear processing of a multicomponent communication signal by combination-sensitive neurons in the anuran inferior colliculus. J Comp Physiol A 203, 749–772 (2017). https://doi.org/10.1007/s00359-017-1195-3

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