Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
???displayArticle.abstract???
The vertebrate hindbrain includes neural circuits that govern essential functions including breathing, blood pressure and heart rate. Hindbrain circuits also participate in generating rhythmic motor patterns for vocalization. In most tetrapods, sound production is powered by expiration and the circuitry underlying vocalization and respiration must be linked. Perception and arousal are also linked; acoustic features of social communication sounds-for example, a baby's cry-can drive autonomic responses. The close links between autonomic functions that are essential for life and vocal expression have been a major in vivo experimental challenge. Xenopus provides an opportunity to address this challenge using an ex vivo preparation: an isolated brain that generates vocal and breathing patterns. The isolated brain allows identification and manipulation of hindbrain vocal circuits as well as their activation by forebrain circuits that receive sensory input, initiate motor patterns and control arousal. Advances in imaging technologies, coupled to the production of Xenopus lines expressing genetically encoded calcium sensors, provide powerful tools for imaging neuronal patterns in the entire fictively behaving brain, a goal of the BRAIN Initiative. Comparisons of neural circuit activity across species (comparative neuromics) with distinctive vocal patterns can identify conserved features, and thereby reveal essential functional components.
Figure 1.
Vocal production in Xenopus. (a) Xenopus call while submerged. (b) Air travels through the glottis to the lungs. The glottis is closed during vocalization. Each sound pulse is generated by separation of paired arytenoids disks (AD), in response to contraction of laryngeal muscles (LM) driven by activity on the vocal nerve (VN). (c) Nerve activity patterns (lower traces) match the sexually differentiated patterns of sound pulses (upper traces) in the male advertisement call and the sexually unreceptive female ticking call
Figure 2.
Fictive calling and breathing preparations in X. laevis. (a) The isolated (ex vivo) brain viewed from above (dorsally) from olfactory bulb rostrally (left) to the end of the hindbrain caudally (right). The most caudal rootlet of cranial nerve IX-X (indicated by the line) contains the axons of motor neurons that innervate glottal, laryngeal and heart muscles and comprises the vocal nerve. (b) Fictive advertisement calling (upper trace) can be recorded from the VN when the neuromodulator serotonin is bath applied to the ex vivo brain. The pattern of VN activity follows the pattern of a male advertisement call (lower trace). (c) Fictive ticking (upper trace) can be recorded from the VN when the neuromodulator serotonin is bath applied to the ex vivo brain. The pattern of VN activity follows the pattern of female ticking (lower trace). (from Rhodes et al., 2007). (d) The isolated (ex vivo) brain and innervated larynx viewed from above A branch of cranial nerve IX-X enters the larynx caudally and contains the axons of motor neurons that innervate glottal and laryngeal muscles. e Recordings from glottal muscles (lower panel; also see Figure 1b) reveal spontaneous bursts of activity that correspond to activity of hindbrain glottal motor neurons. This activity pattern produces the opening of the glottis that allows air to travel from the mouth through the larynx to the lungs and is thus termed fictive breathing
Figure 4.
Molecular identity of forebrain nuclei that contribute to vocal initiation. (a) and (b) are modified from “Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transition,†by Moreno and Gonzalez, 2007, Journal of Anatomy, 211, p 151. (c-e) are modified from “The Xenopus amygdala mediates socially appropriate vocal communication signals.†by Hall et al., 2013, The Journal of Neuroscience, 33, p 14534. (a) The anuran amygdaloid complex in a transverse hemisection of the caudal forebrain illustrating component nuclei, including descending projections to the brainstem (hindbrain); medial is to the right and dorsal is up. (b) A schematic hemisection corresponding to a and illustrating expression of a number of transcription factors (Isl1, Nkx2.1, Lhx7, Lhx1,Dll4), neurotransmitters or neuromodulators (GABA, TH,SP and ENK) and a calcium-binding protein (CR). Note the widespread distribution of the inhibitory neurotransmitter GABA within the CeA. Expression of these molecular markers corresponds to similar patterns in mammals (not included). (c) A fictive advertisement call recorded from the VN after microstimulation in the EA. (d) Effective (red, asterisks) and ineffective (black) stimulation sites for evoking fictive advertisement calls. (e) Comparison of temporal features (fast and slow trill) recorded from an advertisement calling male (in vivo), a fictively advertisement calling male brain (ex vivo), and following EA microstimulation (ex vivo EA stim) indicates that EA activity can initiate a specific fictive call pattern
Figure 5.
Examples of vocal circuit comparisons across and within Xenopus clades. The S, L, and M clades use different genetic mechanisms for primary sex determination. Comparison of neural circuit elementsâusing a fictively calling preparationâacross species from these clades should reveal common and diverged neural circuit mechanisms. Divergence time estimates of Silurana and Xenopus based on Canatella (2015). Phylogeny simplified from Evans et al. (2015)
Ahrens,
Whole-brain functional imaging at cellular resolution using light-sheet microscopy.
2013, Pubmed
Ahrens,
Whole-brain functional imaging at cellular resolution using light-sheet microscopy.
2013,
Pubmed
Albersheim-Carter,
Testing the evolutionary conservation of vocal motoneurons in vertebrates.
2016,
Pubmed
Bass,
Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment.
2008,
Pubmed
Blum,
Xenopus, an ideal model system to study vertebrate left-right asymmetry.
2009,
Pubmed
,
Xenbase
Brahic,
Vocal circuitry in Xenopus laevis: telencephalon to laryngeal motor neurons.
2003,
Pubmed
,
Xenbase
Buzsáki,
Memory, navigation and theta rhythm in the hippocampal-entorhinal system.
2013,
Pubmed
Cannatella,
Xenopus in Space and Time: Fossils, Node Calibrations, Tip-Dating, and Paleobiogeography.
2015,
Pubmed
,
Xenbase
Dick,
Pontine respiratory neurons in anesthetized cats.
1994,
Pubmed
Dunn,
Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion.
2016,
Pubmed
Dunn,
Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish.
2016,
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
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,
"Singing" Fish Rely on Circadian Rhythm and Melatonin for the Timing of Nocturnal Courtship Vocalization.
2016,
Pubmed
Furman,
Sequential Turnovers of Sex Chromosomes in African Clawed Frogs (Xenopus) Suggest Some Genomic Regions Are Good at Sex Determination.
2016,
Pubmed
,
Xenbase
Gjorgjieva,
Computational implications of biophysical diversity and multiple timescales in neurons and synapses for circuit performance.
2016,
Pubmed
Gurdon,
The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes.
2000,
Pubmed
,
Xenbase
Hage,
On the role of the pontine brainstem in vocal pattern generation: a telemetric single-unit recording study in the squirrel monkey.
2006,
Pubmed
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
Katz,
Phylogenetic plasticity in the evolution of molluscan neural circuits.
2016,
Pubmed
Koide,
Xenopus as a model system to study transcriptional regulatory networks.
2005,
Pubmed
,
Xenbase
Leininger,
Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls.
2013,
Pubmed
,
Xenbase
Leininger,
Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus).
2015,
Pubmed
,
Xenbase
Lin,
Genetically encoded indicators of neuronal activity.
2016,
Pubmed
Ma,
Stimulation of the basal and central amygdala in the mustached bat triggers echolocation and agonistic vocalizations within multimodal output.
2014,
Pubmed
Mawaribuchi,
Sex chromosome differentiation and the W- and Z-specific loci in Xenopus laevis.
2017,
Pubmed
,
Xenbase
Missaghi,
The neural control of respiration in lampreys.
2016,
Pubmed
Moreno,
Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transition.
2007,
Pubmed
Muto,
Calcium Imaging of Neuronal Activity in Free-Swimming Larval Zebrafish.
2016,
Pubmed
Nakai,
A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein.
2001,
Pubmed
Pearl,
Development of Xenopus resource centers: the National Xenopus Resource and the European Xenopus Resource Center.
2012,
Pubmed
,
Xenbase
Pérez,
Androgen receptor mRNA expression in Xenopus laevis CNS: sexual dimorphism and regulation in laryngeal motor nucleus.
1996,
Pubmed
,
Xenbase
Potter,
Androgen-induced vocal transformation in adult female African clawed frogs.
2005,
Pubmed
,
Xenbase
Prevedel,
Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy.
2014,
Pubmed
Rhodes,
Xenopus vocalizations are controlled by a sexually differentiated hindbrain central pattern generator.
2007,
Pubmed
,
Xenbase
Rhodes,
Male-male clasping may be part of an alternative reproductive tactic in Xenopus laevis.
2014,
Pubmed
,
Xenbase
Roco,
Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis.
2015,
Pubmed
,
Xenbase
Schmidt,
Breathtaking Songs: Coordinating the Neural Circuits for Breathing and Singing.
2016,
Pubmed
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
Smith,
Brainstem respiratory networks: building blocks and microcircuits.
2013,
Pubmed
Tian,
Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators.
2009,
Pubmed
Tobias,
Vocalizations by a sexually dimorphic isolated larynx: peripheral constraints on behavioral expression.
1987,
Pubmed
,
Xenbase
Tobias,
Vocal communication between male Xenopus laevis.
2004,
Pubmed
,
Xenbase
Tobias,
Evolution of advertisement calls in African clawed frogs.
2011,
Pubmed
,
Xenbase
Tomer,
Advanced CLARITY for rapid and high-resolution imaging of intact tissues.
2014,
Pubmed
Tomer,
SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function.
2015,
Pubmed
Wallen,
The Organizational Hypothesis: Reflections on the 50th anniversary of the publication of Phoenix, Goy, Gerall, and Young (1959).
2009,
Pubmed
Wang,
Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain.
2003,
Pubmed
Wühr,
The Nuclear Proteome of a Vertebrate.
2015,
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,
Rhythm generation, coordination, and initiation in the vocal pathways of male African clawed frogs.
2017,
Pubmed
,
Xenbase
Yartsev,
Grid cells without theta oscillations in the entorhinal cortex of bats.
2011,
Pubmed
Zornik,
Coding rate and duration of vocalizations of the frog, Xenopus laevis.
2012,
Pubmed
,
Xenbase
Zornik,
Regulation of respiratory and vocal motor pools in the isolated brain of Xenopus laevis.
2008,
Pubmed
,
Xenbase
Zornik,
NMDAR-dependent control of call duration in Xenopus laevis.
2010,
Pubmed
,
Xenbase
Zornik,
A neuroendocrine basis for the hierarchical control of frog courtship vocalizations.
2011,
Pubmed
,
Xenbase
