Breathtaking Songs: Coordinating the Neural Circuits for Breathing and Singing.

The vocal behavior of birds is remarkable for its diversity, and songs can feature elaborate characteristics such as long duration, rapid temporal pattern, and broad frequency range. The respiratory system plays a central role in generating the complex song patterns that must be integrated with its life-sustaining functions. Here, we explore how precise coordination between the neural circuits for breathing and singing is fundamental to production of these remarkable behaviors.

[1]  Donald R McCrimmon,et al.  Central pathways of pulmonary and lower airway vagal afferents. , 2006, Journal of applied physiology.

[2]  Alexander Hanuschkin,et al.  Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex , 2016, Neuron.

[3]  Sam E Benezra,et al.  Supplemental Information Population-level Representation of a Temporal Sequence Underlying Song Production in the Zebra Finch , 2022 .

[4]  Richard Hans Robert Hahnloser,et al.  An ultra-sparse code underliesthe generation of neural sequences in a songbird , 2002, Nature.

[5]  J Martin Wild,et al.  Functional Neuroanatomy of the Sensorimotor Control of Singing , 2004, Annals of the New York Academy of Sciences.

[6]  S. Nowicki,et al.  Chapter 11 – Performance limits on birdsong , 2004 .

[7]  Robin C. Ashmore,et al.  Bottom-Up Activation of the Vocal Motor Forebrain by the Respiratory Brainstem , 2008, The Journal of Neuroscience.

[8]  Jakob N. Foerster,et al.  Control of Vocal and Respiratory Patterns in Birdsong: Dissection of Forebrain and Brainstem Mechanisms Using Temperature , 2011, PloS one.

[9]  R. Suthers,et al.  Bilateral coordination and the motor basis of female preference for sexual signals in canary song , 2012, Journal of Experimental Biology.

[10]  Zhiyi Chi,et al.  Temporal Precision and Temporal Drift in Brain and Behavior of Zebra Finch Song , 2001, Neuron.

[11]  H. Seung,et al.  Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances. , 2007, Journal of neurophysiology.

[12]  M. Fee,et al.  Singing-related activity of identified HVC neurons in the zebra finch. , 2007, Journal of neurophysiology.

[13]  G. Mindlin,et al.  Motor control of sound frequency in birdsong involves the interaction between air sac pressure and labial tension. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Michael S. Brainard,et al.  Auditory feedback in learning and maintenance of vocal behaviour , 2000, Nature Reviews Neuroscience.

[15]  F. Goller,et al.  Motor Correlates of Vocal Diversity in Songbirds , 1997 .

[16]  D. Margoliash,et al.  A Mechanism for Frequency Modulation in Songbirds Shared with Humans , 2013, The Journal of Neuroscience.

[17]  M. Coleman,et al.  Recovery of impaired songs following unilateral but not bilateral lesions of nucleus uvaeformis of adult zebra finches. , 2005, Journal of neurobiology.

[18]  Michale S Fee,et al.  Learning to breathe and sing: development of respiratory-vocal coordination in young songbirds. , 2011, Journal of neurophysiology.

[19]  Franz Goller,et al.  A circular model for song motor control in Serinus canaria , 2015, Front. Comput. Neurosci..

[20]  Michale S Fee,et al.  A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors , 2009, Proceedings of the National Academy of Sciences.

[21]  Bruce R Donald,et al.  Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches , 2014, eLife.

[22]  C. Scharff,et al.  The songbird syrinx morphome: a three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ , 2013, BMC Biology.

[23]  Ezequiel M. Arneodo,et al.  Prosthetic Avian Vocal Organ Controlled by a Freely Behaving Bird Based on a Low Dimensional Model of the Biomechanical Periphery , 2012, PLoS Comput. Biol..

[24]  Marc F. Schmidt,et al.  Characterization of respiratory neurons in the rostral ventrolateral medulla, an area critical for vocal production in songbirds. , 2013, Journal of neurophysiology.

[25]  Gert Holstege,et al.  Motor organization of positive and negative emotional vocalization in the cat midbrain periaqueductal gray , 2016, The Journal of comparative neurology.

[26]  D. Margoliash,et al.  The effects of delayed auditory feedback revealed by bone conduction microphone in adult zebra finches , 2015, Scientific Reports.

[27]  E. Nordeen,et al.  Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. , 1992, Behavioral and neural biology.

[28]  Timothy Q Gentner,et al.  Inhibition and recurrent excitation in a computational model of sparse bursting in song nucleus HVC. , 2009, Journal of neurophysiology.

[29]  Robin C. Ashmore,et al.  Bilateral Control and Interhemispheric Coordination in the Avian Song Motor System , 2004, Annals of the New York Academy of Sciences.

[30]  G. Mindlin,et al.  Interaction between telencephalic signals and respiratory dynamics in songbirds. , 2012, Journal of neurophysiology.

[31]  Franz Goller,et al.  Somatosensory feedback modulates the respiratory motor program of crystallized birdsong , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Goodson,et al.  Mammal-Like Organization of the Avian Midbrain Central Gray and a Reappraisal of the Intercollicular Nucleus , 2011, PloS one.

[33]  F. Goller,et al.  Disrupting vagal feedback affects birdsong motor control , 2010, Journal of Experimental Biology.

[34]  Ilya A. Rybak,et al.  Structural and functional architecture of respiratory networks in the mammalian brainstem , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[35]  Franz Goller,et al.  Respiratory patterns and oxygen consumption in singing zebra finches , 2003, Journal of Experimental Biology.

[36]  Bartholomew J. Bacak,et al.  Control of breathing by interacting pontine and pulmonary feedback loops , 2013, BMC Neuroscience.

[37]  Michael A Long,et al.  Motor Origin of Precise Synaptic Inputs onto Forebrain Neurons Driving a Skilled Behavior , 2015, The Journal of Neuroscience.

[38]  M. Brainard,et al.  Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong , 2007, Nature.

[39]  M. Konishi.  The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[40]  F. Goller,et al.  Peripheral mechanisms for vocal production in birds – differences and similarities to human speech and singing , 2010, Brain and Language.

[41]  C. Elemans,et al.  The Singer and the Song: the Neuromechanics of Avian Sound Production This Review Comes from a Themed Issue on Communication and Language Sound Production Physiology Muscle Function in Motor Control Synergistic Motor Control , 2022 .

[42]  Jeffrey Podos,et al.  A PERFORMANCE CONSTRAINT ON THE EVOLUTION OF TRILLED VOCALIZATIONS IN A SONGBIRD FAMILY (PASSERIFORMES: EMBERIZIDAE) , 1997, Evolution; international journal of organic evolution.

[43]  Yonatan Sanz Perl,et al.  Elemental gesture dynamics are encoded by song premotor cortical neurons , 2013, Nature.

[44]  J. Brackenbury.  A comparison of the origin and temporal arrangement of pulsed sounds in the songs of the Grasshopper and Sedge warblers, Locustella naevia and Acrocephalus schoenobaenus , 2009 .

[45]  M. Fee,et al.  Using temperature to analyze temporal dynamics in the songbird motor pathway , 2008, Nature.

[46]  F. J. Clark,et al.  On the regulation of depth and rate of breathing , 1972, The Journal of physiology.

[47]  Marc F. Schmidt,et al.  Testing the evolutionary conservation of vocal motoneurons in vertebrates , 2016, Respiratory Physiology & Neurobiology.

[48]  E.C.L. Vu,et al.  Identification of a forebrain motor programming network for the learned song of zebra finches , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  G. Holstege,et al.  Stimulation of the Midbrain Periaqueductal Gray Modulates Preinspiratory Neurons in the Ventrolateral Medulla in the Rat In Vivo , 2013, The Journal of comparative neurology.

[50]  F Goller,et al.  Inspiratory muscle activity during bird song. , 1998, Journal of neurobiology.

[51]  F Goller,et al.  The metabolic cost of birdsong production. , 2001, The Journal of experimental biology.

[52]  I. Rybak,et al.  Learning to breathe: control of the inspiratory–expiratory phase transition shifts from sensory‐ to central‐dominated during postnatal development in rats , 2009, The Journal of physiology.

[53]  Richard Mooney,et al.  Neural mechanisms for learned birdsong. , 2009, Learning & memory.

[54]  Kosuke Hamaguchi,et al.  A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations , 2016, Neuron.

[55]  J. Švec,et al.  Universal mechanisms of sound production and control in birds and mammals , 2015, Nature Communications.

[56]  I. Rybak,et al.  Respiratory Rhythm Entrainment by Somatic Afferent Stimulation , 2005, The Journal of Neuroscience.

[57]  Y. Nakajima,et al.  Role of pulmonary afferent inputs in vocal on-switch in the cat , 1997, Neuroscience Research.

[58]  Marc F. Schmidt,et al.  The respiratory-vocal system of songbirds: anatomy, physiology, and neural control. , 2014, Progress in brain research.

[59]  F. Goller,et al.  Integrative physiology of fundamental frequency control in birds , 2013, Journal of Physiology-Paris.

[60]  G. Holstege,et al.  Periaqueductal gray control of breathing. , 2010, Advances in experimental medicine and biology.

[61]  J. Feldman,et al.  Understanding the rhythm of breathing: so near, yet so far. , 2013, Annual review of physiology.

[62]  Franz Goller,et al.  Temperature Induced Syllable Breaking Unveils Nonlinearly Interacting Timescales in Birdsong Motor Pathway , 2013, PloS one.

[63]  R. Suthers.  Chapter 9 – How birds sing and why it matters , 2004 .

[64]  Tobias Riede,et al.  The acoustic effect of vocal tract adjustments in zebra finches , 2012, Journal of Comparative Physiology A.

[65]  G. Holstege,et al.  The midbrain periaqueductal gray changes the eupneic respiratory rhythm into a breathing pattern necessary for survival of the individual and of the species. , 2014, Progress in brain research.

[66]  M. Smotherman,et al.  Sensory feedback control of mammalian vocalizations , 2007, Behavioural Brain Research.

[67]  A. Doupe,et al.  Translating birdsong: songbirds as a model for basic and applied medical research. , 2013, Annual review of neuroscience.

[68]  R. Suthers,et al.  Airflow and pressure during canary song: direct evidence for mini-breaths , 2004, Journal of Comparative Physiology A.

[69]  Dezhe Z. Jin,et al.  Support for a synaptic chain model of neuronal sequence generation , 2010, Nature.

[70]  R. Bandler,et al.  Pulmonary and upper airway afferent influences on the motor pattern of vocalization evoked by excitation of the midbrain periaqueductal gray of the cat , 1993, Brain Research.

[71]  Franz Goller,et al.  Frequency modulation during song in a suboscine does not require vocal muscles. , 2008, Journal of neurophysiology.