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Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication

Darcy B. Kelley, Irene H. Ballagh, Charlotte L. Barkan, Andres Bendesky, Taffeta M. Elliott, Ben J. Evans, Ian C. Hall, Young Mi Kwon, Ursula Kwong-Brown, Elizabeth C. Leininger, Emilie C. Perez, Heather J. Rhodes, Avelyne Villain, Ayako Yamaguchi and Erik Zornik
Journal of Neuroscience 2 January 2020, 40 (1) 22-36; DOI: https://doi.org/10.1523/JNEUROSCI.0736-19.2019
Darcy B. Kelley
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
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Irene H. Ballagh
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
2Department of Zoology, University of British Columbia, Vancouver V6T132, Canada,
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Charlotte L. Barkan
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
3Department of Biology, Reed College, Portland, Oregon 97202,
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Andres Bendesky
4Department of Ecology, Evolution and Environmental Biology and Zuckerman Mind, Brain, Behavior Institute, Columbia University, New York, New York 10027,
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Taffeta M. Elliott
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
5Department of Psychology and Education, New Mexico Institute of Mining and Technology, Socorro, New Mexico 87801,
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Ben J. Evans
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
7Department of Biology, McMaster University, Hamilton, Ontario L8S 4L8, Canada,
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Ian C. Hall
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
8Department of Biology, Benedictine University, Lisle, Illinois 60532,
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Young Mi Kwon
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
4Department of Ecology, Evolution and Environmental Biology and Zuckerman Mind, Brain, Behavior Institute, Columbia University, New York, New York 10027,
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Ursula Kwong-Brown
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
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Elizabeth C. Leininger
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
6Division of Natural Sciences, New College of Florida, Sarasota, Florida 34243,
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Emilie C. Perez
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
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Heather J. Rhodes
9Department of Biology, Boston University, Boston, Massachusetts 02215,
10Department of Biology, Denison University, Granville, Ohio 43023, and
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Avelyne Villain
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
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Ayako Yamaguchi
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
9Department of Biology, Boston University, Boston, Massachusetts 02215,
11School of Biological Sciences, University of Utah, Salt Lake City, Utah 84112
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Erik Zornik
1Department of Biological Sciences and Program in Neurobiology and Behavior, Columbia University, New York, New York 10027,
3Department of Biology, Reed College, Portland, Oregon 97202,
9Department of Biology, Boston University, Boston, Massachusetts 02215,
11School of Biological Sciences, University of Utah, Salt Lake City, Utah 84112
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Abstract

In many species, vocal communication is essential for coordinating social behaviors including courtship, mating, parenting, rivalry, and alarm signaling. Effective communication requires accurate production, detection, and classification of signals, as well as selection of socially appropriate responses. Understanding how signals are generated and how acoustic signals are perceived is key to understanding the neurobiology of social behaviors. Here we review our long-standing research program focused on Xenopus, a frog genus which has provided valuable insights into the mechanisms and evolution of vertebrate social behaviors. In Xenopus laevis, vocal signals differ between the sexes, through development, and across the genus, reflecting evolutionary divergence in sensory and motor circuits that can be interrogated mechanistically. Using two ex vivo preparations, the isolated brain and vocal organ, we have identified essential components of the vocal production system: the sexually differentiated larynx at the periphery, and the hindbrain vocal central pattern generator (CPG) centrally, that produce sex- and species-characteristic sound pulse frequencies and temporal patterns, respectively. Within the hindbrain, we have described how intrinsic membrane properties of neurons in the vocal CPG generate species-specific vocal patterns, how vocal nuclei are connected to generate vocal patterns, as well as the roles of neurotransmitters and neuromodulators in activating the circuit. For sensorimotor integration, we identified a key forebrain node that links auditory and vocal production circuits to match socially appropriate vocal responses to acoustic features of male and female calls. The availability of a well supported phylogeny as well as reference genomes from several species now support analysis of the genetic architecture and the evolutionary divergence of neural circuits for vocal communication. Xenopus thus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution. As one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems, Xenopus provides insights that can inform social communication across phyla.

  • duets
  • song
  • hindbrain
  • CPG
  • neuroendocrine
  • parabrachial
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The Journal of Neuroscience: 40 (1)
Journal of Neuroscience
Vol. 40, Issue 1
2 Jan 2020
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Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication
Darcy B. Kelley, Irene H. Ballagh, Charlotte L. Barkan, Andres Bendesky, Taffeta M. Elliott, Ben J. Evans, Ian C. Hall, Young Mi Kwon, Ursula Kwong-Brown, Elizabeth C. Leininger, Emilie C. Perez, Heather J. Rhodes, Avelyne Villain, Ayako Yamaguchi, Erik Zornik
Journal of Neuroscience 2 January 2020, 40 (1) 22-36; DOI: 10.1523/JNEUROSCI.0736-19.2019

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Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication
Darcy B. Kelley, Irene H. Ballagh, Charlotte L. Barkan, Andres Bendesky, Taffeta M. Elliott, Ben J. Evans, Ian C. Hall, Young Mi Kwon, Ursula Kwong-Brown, Elizabeth C. Leininger, Emilie C. Perez, Heather J. Rhodes, Avelyne Villain, Ayako Yamaguchi, Erik Zornik
Journal of Neuroscience 2 January 2020, 40 (1) 22-36; DOI: 10.1523/JNEUROSCI.0736-19.2019
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Keywords

  • duets
  • song
  • hindbrain
  • CPG
  • neuroendocrine
  • parabrachial

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