XB-ART-56610
J Neurosci
2020 Jan 02;401:22-36. doi: 10.1523/JNEUROSCI.0736-19.2019.
Show Gene links
Show Anatomy links
Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication.
Kelley DB
,
Ballagh IH
,
Barkan CL
,
Bendesky A
,
Elliott TM
,
Evans BJ
,
Hall IC
,
Kwon YM
,
Kwong-Brown U
,
Leininger EC
,
Perez EC
,
Rhodes HJ
,
Villain A
,
Yamaguchi A
,
Zornik E
.
???displayArticle.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.
???displayArticle.pubmedLink??? 31896561
???displayArticle.pmcLink??? PMC6939475
???displayArticle.link??? J Neurosci
???displayArticle.grants??? [+]
F32 NS054391 NINDS NIH HHS , F32 GM103266 NIGMS NIH HHS , R01 NS048834 NINDS NIH HHS , F31 DC006743 NIDCD NIH HHS , R01 NS023684 NINDS NIH HHS , Howard Hughes Medical Institute , R15 NS091977 NINDS NIH HHS
References [+] :
Albersheim-Carter,
Testing the evolutionary conservation of vocal motoneurons in vertebrates.
2016, Pubmed
Albersheim-Carter, Testing the evolutionary conservation of vocal motoneurons in vertebrates. 2016, Pubmed
Baertsch, The interdependence of excitation and inhibition for the control of dynamic breathing rhythms. 2018, Pubmed
Barkan, Evolution of vocal patterns: tuning hindbrain circuits during species divergence. 2017, Pubmed , Xenbase
Barkan, Feedback to the future: motor neuron contributions to central pattern generator function. 2019, Pubmed
Barkan, Premotor Neuron Divergence Reflects Vocal Evolution. 2018, Pubmed , Xenbase
Bass, Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. 2008, Pubmed
Baur, Sexually differentiated, androgen-regulated, larynx-specific myosin heavy-chain isoforms in Xenopus tropicalis; comparison to Xenopus laevis. 2008, Pubmed , Xenbase
Bendesky, The genetic basis of parental care evolution in monogamous mice. 2017, Pubmed
Billeter, Control of male sexual behavior in Drosophila by the sex determination pathway. 2006, Pubmed
Bopp, Sex determination in insects: variations on a common theme. 2014, Pubmed
Brahic, Vocal circuitry in Xenopus laevis: telencephalon to laryngeal motor neurons. 2003, Pubmed , Xenbase
Cannatella, Xenopus in Space and Time: Fossils, Node Calibrations, Tip-Dating, and Paleobiogeography. 2015, Pubmed , Xenbase
Catz, Sexually dimorphic expression of a laryngeal-specific, androgen-regulated myosin heavy chain gene during Xenopus laevis development. 1992, Pubmed , Xenbase
Christensen-Dalsgaard, Biophysics of underwater hearing in the clawed frog, Xenopus laevis. 1995, Pubmed , Xenbase
Cinelli, Neuronal mechanisms of respiratory pattern generation are evolutionary conserved. 2013, Pubmed
Del Negro, Breathing matters. 2018, Pubmed
Dick, Pontine respiratory neurons in anesthetized cats. 1994, Pubmed
Ding, Natural courtship song variation caused by an intronic retroelement in an ion channel gene. 2016, Pubmed
Dunlap, Estrogen modifies an electrocommunication signal by altering the electrocyte sodium current in an electric fish, Sternopygus. 1997, Pubmed
Edwards, Auditory and lateral line inputs to the midbrain of an aquatic anuran: neuroanatomic studies in Xenopus laevis. 2001, Pubmed , Xenbase
Elemans, Universal mechanisms of sound production and control in birds and mammals. 2015, Pubmed
Elliott, Male discrimination of receptive and unreceptive female calls by temporal features. 2007, Pubmed , Xenbase
Elliott, Temporally selective processing of communication signals by auditory midbrain neurons. 2011, Pubmed , Xenbase
Elliott, Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis. 2007, Pubmed , Xenbase
Evans, Description of a new octoploid frog species (Anura: Pipidae: Xenopus) from the Democratic Republic of the Congo, with a discussion of the biogeography of African clawed frogs in the Albertine Rift. 2011, Pubmed , Xenbase
Evans, Xenopus fraseri: Mr. Fraser, where did your frog come from? 2019, Pubmed , Xenbase
Evans, Evolution of RAG-1 in polyploid clawed frogs. 2005, Pubmed , Xenbase
Evans, Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa. 2015, Pubmed , Xenbase
Feng, Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. 2017, Pubmed
Feng, "Singing" Fish Rely on Circadian Rhythm and Melatonin for the Timing of Nocturnal Courtship Vocalization. 2016, Pubmed
Ferrari, Individual variation in and androgen-modulation of the sodium current in electric organ. 1995, Pubmed
Fischer, Androgen-directed development of the Xenopus laevis larynx: control of androgen receptor expression and tissue differentiation. 1995, Pubmed , Xenbase
Franklin, Prefrontal cortical control of a brainstem social behavior circuit. 2017, Pubmed
Furman, Pan-African phylogeography of a model organism, the African clawed frog 'Xenopus laevis'. 2015, Pubmed , Xenbase
Goaillard, Functional consequences of animal-to-animal variation in circuit parameters. 2009, Pubmed
Gurdon, The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. 2000, Pubmed , Xenbase
Hall, The Xenopus amygdala mediates socially appropriate vocal communication signals. 2013, Pubmed , Xenbase
Hall, Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus). 2016, Pubmed , Xenbase
Hannigan, Androgen-induced alterations in vocalizations of female Xenopus laevis: modifiability and constraints. 1986, Pubmed , Xenbase
Hollis, Distribution of GABA-like immunoreactive cell bodies in the brains of two amphibians, Rana catesbeiana and Xenopus laevis. 2005, Pubmed , Xenbase
Irisarri, Reversal to air-driven sound production revealed by a molecular phylogeny of tongueless frogs, family Pipidae. 2011, Pubmed
Jacobson, Cell lineage analysis of neural induction: origins of cells forming the induced nervous system. 1984, Pubmed , Xenbase
Katz, Evolution of central pattern generators and rhythmic behaviours. 2016, Pubmed
Kay, Trophic effects of androgen: development and hormonal regulation of neuron number in a sexually dimorphic vocal motor nucleus. 1999, Pubmed , Xenbase
Kelley, Development and hormone regulation of androgen receptor levels in the sexually dimorphic larynx of Xenopus laevis. 1989, Pubmed , Xenbase
Kelley, Auditory and vocal nuclei in the frog brain concentrate sex hormones. 1980, Pubmed , Xenbase
Kelley, Female sex behaviors in the South African clawed frog, Xenopus laevis: gonadotropin-releasing, gonadotropic, and steroid hormones. 1982, Pubmed , Xenbase
Kiehn, Decoding the organization of spinal circuits that control locomotion. 2016, Pubmed
Kwong-Brown, The return to water in ancestral Xenopus was accompanied by a novel mechanism for producing and shaping vocal signals. 2019, Pubmed , Xenbase
Lawton, Motor Neurons Tune Premotor Activity in a Vertebrate Central Pattern Generator. 2017, Pubmed , Xenbase
Leininger, Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus). 2015, Pubmed , Xenbase
Leininger, Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls. 2013, Pubmed , Xenbase
Lindstedt, Krogh 1929 or 'the Krogh principle'. 2014, Pubmed
Lutz, Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation. 2001, Pubmed , Xenbase
Mallet, Hybrid speciation. 2007, Pubmed
Marder, Central pattern generators and the control of rhythmic movements. 2001, Pubmed
Marin, Hormone-sensitive stages in the sexual differentiation of laryngeal muscle fiber number in Xenopus laevis. 1990, Pubmed , Xenbase
Mason, STRUCTURE AND FUNCTION OF THE MIDDLE EAR APPARATUS OF THE AQUATIC FROG, XENOPUS LAEVIS. 2009, Pubmed , Xenbase
Mason, Song evolution, speciation, and vocal learning in passerine birds. 2017, Pubmed
Mesgarani, Phonetic feature encoding in human superior temporal gyrus. 2014, Pubmed
Milton, The Xenopus Pregnancy Test. 1946, Pubmed , Xenbase
Missaghi, The neural control of respiration in lampreys. 2016, Pubmed
Mitra, The circuit architecture of whole brains at the mesoscopic scale. 2014, Pubmed
Moreno, Characterization of the bed nucleus of the stria terminalis in the forebrain of anuran amphibians. 2012, Pubmed , Xenbase
Moreno, Central amygdala in anuran amphibians: neurochemical organization and connectivity. 2005, Pubmed , Xenbase
Morrell, Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian, Xenopus laevis. II. Estradiol. 1975, Pubmed , Xenbase
Nasipak, Developing laryngeal muscle of Xenopus laevis as a model system: androgen-driven myogenesis controls fiber type transformation. 2012, Pubmed , Xenbase
O'Connell, Evolution of a vertebrate social decision-making network. 2012, Pubmed
Onimaru, Midline section of the medulla abolishes inspiratory activity and desynchronizes pre-inspiratory neuron rhythm on both sides of the medulla in newborn rats. 2015, Pubmed
Paton, Mapping the auditory central nervous system of Xenopus laevis with 2-deoxyglucose autoradiography. 1982, Pubmed , Xenbase
Pérez, Androgen receptor mRNA expression in Xenopus laevis CNS: sexual dimorphism and regulation in laryngeal motor nucleus. 1996, Pubmed , Xenbase
PHOENIX, Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. 1959, Pubmed
Potter, Androgen-induced vocal transformation in adult female African clawed frogs. 2005, Pubmed , Xenbase
Quintana, A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: functional aspects revealed by glutamate stimulation. 2011, Pubmed
Ravignani, Interactive rhythms across species: the evolutionary biology of animal chorusing and turn-taking. 2019, Pubmed
Rhodes, Xenopus vocalizations are controlled by a sexually differentiated hindbrain central pattern generator. 2007, Pubmed , Xenbase
Robertson, Androgen directs sexual differentiation of laryngeal innervation in developing Xenopus laevis. 1994, Pubmed , Xenbase
Ruel, Facilitation at the sexually differentiated laryngeal synapse of Xenopus laevis. 1998, Pubmed , Xenbase
Sassoon, Androgen regulation of muscle fiber type in the sexually dimorphic larynx of Xenopus laevis. 1987, Pubmed , Xenbase
Sassoon, Androgen-induced myogenesis and chondrogenesis in the larynx of Xenopus laevis. 1986, Pubmed , Xenbase
Session, Genome evolution in the allotetraploid frog Xenopus laevis. 2016, Pubmed , Xenbase
Simpson, Origin and identification of fibers in the cranial nerve IX-X complex of Xenopus laevis: Lucifer Yellow backfills in vitro. 1986, Pubmed , Xenbase
Smotherman, A mechanism for vocal-respiratory coupling in the mammalian parabrachial nucleus. 2006, Pubmed
Sweeney, Harnessing vocal patterns for social communication. 2014, Pubmed , Xenbase
Tobias, Vocal communication between male Xenopus laevis. 2004, Pubmed , Xenbase
Tobias, Rapping, a female receptive call, initiates male-female duets in the South African clawed frog. 1998, Pubmed , Xenbase
Tobias, Attaining and maintaining strong vocal synapses in female Xenopus laevis. 1998, Pubmed , Xenbase
Tobias, Evolution of advertisement calls in African clawed frogs. 2011, Pubmed , Xenbase
Tobias, A sex difference in synaptic efficacy at the laryngeal neuromuscular junction of Xenopus laevis. 1995, Pubmed , Xenbase
Tobias, Vocalizations by a sexually dimorphic isolated larynx: peripheral constraints on behavioral expression. 1987, Pubmed , Xenbase
van der Heijden, Loss of Atoh1 from neurons regulating hypoxic and hypercapnic chemoresponses causes neonatal respiratory failure in mice. 2018, Pubmed
Vignal, Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. 2007, Pubmed , Xenbase
Watson, Laryngeal muscle and motor neuron plasticity in Xenopus laevis: testicular masculinization of a developing neuromuscular system. 1993, Pubmed , Xenbase
Wetzel, Androgen and gonadotropin effects on male mate calls in South African clawed frogs, Xenopus laevis. 1983, Pubmed , Xenbase
Wu, Estrogen receptors in Xenopus: duplicate genes, splice variants, and tissue-specific expression. 2003, Pubmed , Xenbase
Wu, Estrogen and laryngeal synaptic strength in Xenopus laevis: opposite effects of acute and chronic exposure. 2001, Pubmed , Xenbase
Xu, The Genetics of Mating Song Evolution Underlying Rapid Speciation: Linking Quantitative Variation to Candidate Genes for Behavioral Isolation. 2019, Pubmed
Yamaguchi, Rhythm generation, coordination, and initiation in the vocal pathways of male African clawed frogs. 2017, Pubmed , Xenbase
Yamaguchi, Generating sexually differentiated vocal patterns: laryngeal nerve and EMG recordings from vocalizing male and female african clawed frogs (Xenopus laevis). 2000, Pubmed , Xenbase
Yamaguchi, Development of an Acute Method to Deliver Transgenes Into the Brains of Adult Xenopus laevis. 2018, Pubmed , Xenbase
Yang, Direct action of gonadotropin in brain integrates behavioral and reproductive functions. 2007, Pubmed , Xenbase
Yin, Satellite cells and the muscle stem cell niche. 2013, Pubmed
Yu, Endogenous serotonin acts on 5-HT2C-like receptors in key vocal areas of the brain stem to initiate vocalizations in Xenopus laevis. 2010, Pubmed , Xenbase
Zornik, Regulation of respiratory and vocal motor pools in the isolated brain of Xenopus laevis. 2008, Pubmed , Xenbase
Zornik, A neuroendocrine basis for the hierarchical control of frog courtship vocalizations. 2011, Pubmed , Xenbase
Zornik, Breathing and calling: neuronal networks in the Xenopus laevis hindbrain. 2007, Pubmed , Xenbase
Zornik, NMDAR-dependent control of call duration in Xenopus laevis. 2010, Pubmed , Xenbase
Zornik, Coding rate and duration of vocalizations of the frog, Xenopus laevis. 2012, Pubmed , Xenbase
Zornik, Vocal pathway degradation in gonadectomized Xenopus laevis adults. 2011, Pubmed , Xenbase