Short Bouts of Vocalization Induce Long-Lasting Fast Gamma Oscillations in a Sensorimotor Nucleus

Performance evaluation is a critical feature of motor learning. In the vocal system, it requires the integration of auditory feedback signals with vocal motor commands. The network activity that supports such integration is unknown, but it has been proposed that vocal performance evaluation occurs offline. Recording from NIf, a sensorimotor structure in the avian song system, we show that short bouts of singing in adult male zebra finches (Taeniopygia guttata) induce persistent increases in firing activity and coherent oscillations in the fast gamma range (90–150 Hz). Single units are strongly phase locked to these oscillations, which can last up to 30 s, often outlasting vocal activity by an order of magnitude. In other systems, oscillations often are triggered by events or behavioral tasks but rarely outlast the event that triggered them by more than 1 s. The present observations are the longest reported gamma oscillations triggered by an isolated behavioral event. In mammals, gamma oscillations have been associated with memory consolidation and are hypothesized to facilitate communication between brain regions. We suggest that the timing and persistent nature of NIf's fast gamma oscillations make them well suited to facilitate the integration of auditory and vocal motor traces associated with vocal performance evaluation.

[1]  W. Singer,et al.  Synchronization of neuronal responses in the optic tectum of awake pigeons , 1996, Visual Neuroscience.

[2]  Jack W. Tsao,et al.  Observed brain dynamics, P.P. Mitra, H. Bokil. Oxford University Press (2008), ISBN-13: 978-0-19-517808-1, 381 pages, $65.00 , 2009 .

[3]  Daniel Margoliash,et al.  Sleep and sensorimotor integration during early vocal learning in a songbird , 2008, Nature.

[4]  Masakazu Konishi,et al.  The Role of Auditory Feedback in Birdsong , 2004, Annals of the New York Academy of Sciences.

[5]  N. Logothetis The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[6]  K. Linkenkaer-Hansen,et al.  Inbred mouse strains differ in multiple hippocampal activity traits , 2009, The European journal of neuroscience.

[7]  Daniel Margoliash,et al.  Sleep, off-line processing, and vocal learning , 2010, Brain and Language.

[8]  Christian K. Machens,et al.  Testing the Efficiency of Sensory Coding with Optimal Stimulus Ensembles , 2005, Neuron.

[9]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[10]  Michael S. Brainard,et al.  Online Contributions of Auditory Feedback to Neural Activity in Avian Song Control Circuitry , 2008, The Journal of Neuroscience.

[11]  A. Leonardo,et al.  Ensemble Coding of Vocal Control in Birdsong , 2005, The Journal of Neuroscience.

[12]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[13]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

[14]  Gustavo Deco,et al.  The Neuronal Basis of Attention: Rate versus Synchronization Modulation , 2008, The Journal of Neuroscience.

[15]  Mitchell Steinschneider,et al.  Coding of repetitive transients by auditory cortex on Heschl's gyrus. , 2009, Journal of neurophysiology.

[16]  J. Fell,et al.  Memory formation by neuronal synchronization , 2006, Brain Research Reviews.

[17]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[18]  G. E. Vates,et al.  Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata) , 1996, The Journal of comparative neurology.

[19]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[20]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[21]  Jessica A. Cardin,et al.  Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. , 2004, Journal of neurophysiology.

[22]  Peter L. Rauske,et al.  State and neuronal class-dependent reconfiguration in the avian song system. , 2003, Journal of neurophysiology.

[23]  W. Singer,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2022 .

[24]  Stephen V. David,et al.  Decoupling Action Potential Bias from Cortical Local Field Potentials , 2010, Comput. Intell. Neurosci..

[25]  Marc F Schmidt,et al.  Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. , 2005, Journal of neurophysiology.

[26]  Masakazu Konishi,et al.  Decrystallization of adult birdsong by perturbation of auditory feedback , 1999, Nature.

[27]  A. Arnold,et al.  Evidence for cholinergic participation in the control of bird song: Acetylcholinesterase distribution and muscarinic receptor autoradiography in the zebra finch brain , 1981, The Journal of comparative neurology.

[28]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

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

[30]  J. Wild,et al.  Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches , 2001, Brain Research.

[31]  Christopher M. Bishop,et al.  Robust Bayesian Mixture Modelling , 2005, ESANN.

[32]  R. Zann The Zebra Finch: A Synthesis of Field and Laboratory Studies , 1996 .

[33]  R. Shapley,et al.  LFP power spectra in V1 cortex: the graded effect of stimulus contrast. , 2005, Journal of neurophysiology.

[34]  F. Nottebohm,et al.  Age at Deafening Affects the Stability of Learned Song in Adult Male Zebra Finches , 2000, The Journal of Neuroscience.

[35]  G. Laurent,et al.  Odorant-induced oscillations in the mushroom bodies of the locust , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[37]  A. C. Yu,et al.  Temporal Hierarchical Control of Singing in Birds , 1996, Science.

[38]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[39]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[40]  R. Mooney,et al.  Calcium‐binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata) , 2005, The Journal of comparative neurology.

[41]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[42]  Richard Mooney,et al.  Song decrystallization in adult zebra finches does not require the song nucleus NIf. , 2009, Journal of neurophysiology.

[43]  Masaaki Nishida,et al.  Cortical gamma-oscillations modulated by listening and overt repetition of phonemes , 2010, NeuroImage.

[44]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[45]  Richard H R Hahnloser,et al.  Sleep-related spike bursts in HVC are driven by the nucleus interface of the nidopallium. , 2007, Journal of neurophysiology.

[46]  D. Vicario,et al.  Brain pathways for learned and unlearned vocalizations differ in zebra finches , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Masakazu Konishi,et al.  New brain pathways found in the vocal control system of a songbird , 2010, The Journal of comparative neurology.

[48]  D Margoliash,et al.  Gradual Emergence of Song Selectivity in Sensorimotor Structures of the Male Zebra Finch Song System , 1999, The Journal of Neuroscience.

[49]  Kazuo Okanoya,et al.  Lesion of a higher‐order song nucleus disrupts phrase level complexity in Bengalese finches , 2000, Neuroreport.

[50]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[51]  Hellmuth Obrig,et al.  Stimulus-Induced and State-Dependent Sustained Gamma Activity Is Tightly Coupled to the Hemodynamic Response in Humans , 2009, The Journal of Neuroscience.

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

[53]  M. Dalva,et al.  Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. , 1999, Journal of neurophysiology.

[54]  J. S. McCasland,et al.  Neuronal control of bird song production , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  E. Bramon,et al.  The early auditory gamma-band response is heritable and a putative endophenotype of schizophrenia. , 2011, Schizophrenia bulletin.

[56]  H. Karten,et al.  Laminar and columnar auditory cortex in avian brain , 2010, Proceedings of the National Academy of Sciences.

[57]  Daniel Margoliash,et al.  Mammalian-like features of sleep structure in zebra finches , 2008, Proceedings of the National Academy of Sciences.

[58]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[59]  P. König,et al.  A Functional Gamma-Band Defined by Stimulus-Dependent Synchronization in Area 18 of Awake Behaving Cats , 2003, The Journal of Neuroscience.

[60]  R. Mooney,et al.  Synaptic Transformations Underlying Highly Selective Auditory Representations of Learned Birdsong , 2004, The Journal of Neuroscience.

[61]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[62]  Sarah M. N. Woolley,et al.  Bengalese Finches Lonchura Striata Domestica Depend upon Auditory Feedback for the Maintenance of Adult Song , 1997, The Journal of Neuroscience.

[63]  D. Thomson,et al.  Spectrum estimation and harmonic analysis , 1982, Proceedings of the IEEE.

[64]  Peter L. Rauske,et al.  Neuronal Stability and Drift across Periods of Sleep: Premotor Activity Patterns in a Vocal Control Nucleus of Adult Zebra Finches , 2010, The Journal of Neuroscience.

[65]  Y. Dan,et al.  Spike Timing-Dependent Plasticity of Neural Circuits , 2004, Neuron.

[66]  H. Williams,et al.  Temporal patterning of song production: participation of nucleus uvaeformis of the thalamus. , 1993, Journal of neurobiology.

[67]  J. Schoffelen,et al.  Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction , 2005, Science.

[68]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[69]  C. Bédard,et al.  Macroscopic models of local field potentials and the apparent 1/f noise in brain activity. , 2008, Biophysical journal.

[70]  D. Margoliash,et al.  Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (taenopygia guttata) , 1992, The Journal of comparative neurology.

[71]  Jessica A. Cardin,et al.  Noradrenergic Inputs Mediate State Dependence of Auditory Responses in the Avian Song System , 2022 .

[72]  Georg B. Keller,et al.  Neural processing of auditory feedback during vocal practice in a songbird , 2009, Nature.