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Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis

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Abstract

The clawed frog Xenopus laevis produces vocalizations consisting of distinct patterns of clicks. This study provides the first description of spontaneous, pure-tone and communication-signal evoked discharge properties of auditory nerve (n.VIII) fibers and dorsal medullary nucleus (DMN) cells in an obligatorily aquatic anuran. Responses of 297 n.VIII and 253 DMN units are analyzed for spontaneous rates (SR), frequency tuning, rate-intensity functions, and firing rate adaptation, with a view to how these basic characteristics shape responses to recorded call stimuli. Response properties generally resemble those in partially terrestrial anurans. Broad tuning exists across characteristic frequencies (CFs). Threshold minima are −101 dB re 1 mm/s at 675 Hz; −87 dB at 1,600 Hz; and −61 dB at 3,000 Hz (−90, −77, and −44 dB re 1 Pa, respectively), paralleling the peak frequency of vocalizations at 1.2–1.6 kHz with ∼500 Hz in 3 dB bandwidth. SRs range from 0 to 80 (n.VIII) and 0 to 73 spikes/s (DMN). Nerve and DMN units of all CFs follow click rates in natural calls, ≤67 clicks/s and faster. Units encode clicks with a single spike, double spikes, or bursts. Spike times correlate closely with click envelopes. No temporal filtering for communicative click rates occurs in either n.VIII or the DMN.

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Abbreviations

ACF:

Autocorrelation function

AM:

Amplitude modulation

AP:

Amphibian papilla

BP:

Basilar papilla

CC:

Cross-correlation maximum

CCF:

Cross-correlation function

CF:

Characteristic frequency

dB:

Decibels

DMN:

Dorsal medullary nucleus

DPOAE:

Distortion product otoacoustic emissions

FTC:

Frequency–threshold curve

n.VIII:

Auditory nerve

PSTH:

Poststimulus time histogram

Q10 :

Tuning quality factor

SR:

Spontaneous rate

TS:

Torus semicircularis

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Acknowledgments

We gratefully acknowledge the help of Morten Kanneworff, Elizabeth Olson, Daniel Salzman, David Vicario, and Sarah Woolley. Martha Tobias made the underwater call recordings used as stimuli. We also thank two anonymous referees for comments, which strengthened the paper. Research and international travel was supported in part by a National Science Foundation graduate fellowship, by a National Institute of Deafness and Communication Disorders NRSA graduate fellowship, by NIH grant NS23684 and by the Danish National Science Foundation. Animal care and use for this study was approved both by the Institutional Animal Care and Use Committee at Columbia University (AC-AAAA1401) and the Danish Animal Experimentation Board (Dyreforsøgstilsynet), grant 1999/561–169. The experiments are legal in both the United States and Denmark, and comply with the “Principles of animal care”, publication No. 86–23, of the National Institute of Health.

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Authors and Affiliations

  1. Neurobiology and Behavior, Columbia University, New York, NY, USA

    Taffeta M. Elliott & Darcy B. Kelley

  2. Institute of Biology, University of Southern Denmark, Odense, Denmark

    Jakob Christensen-Dalsgaard

  3. Biological Sciences, Columbia University, New York, NY, USA

    Darcy B. Kelley

  4. UC Berkeley, Helen Wills Neuroscience Institute, 3210 Tolman Hall, Berkeley, CA, 94720, USA

    Taffeta M. Elliott

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  1. Taffeta M. Elliott
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Correspondence to Taffeta M. Elliott.

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Elliott, T.M., Christensen-Dalsgaard, J. & Kelley, D.B. Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis . J Comp Physiol A 193, 1243–1257 (2007). https://doi.org/10.1007/s00359-007-0285-z

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