Mesoscopic Patterns of Neural Activity Support Songbird Cortical Sequences

Time-locked sequences of neural activity can be found throughout the vertebrate forebrain in various species and behavioral contexts. From “time cells” in the hippocampus of rodents to cortical activity controlling movement, temporal sequence generation is integral to many forms of learned behavior. However, the mechanisms underlying sequence generation are not well known. Here, we describe a spatial and temporal organization of the songbird premotor cortical microcircuit that supports sparse sequences of neural activity. Multi-channel electrophysiology and calcium imaging reveal that neural activity in premotor cortex is correlated with a length scale of 100 µm. Within this length scale, basal-ganglia–projecting excitatory neurons, on average, fire at a specific phase of a local 30 Hz network rhythm. These results show that premotor cortical activity is inhomogeneous in time and space, and that a mesoscopic dynamical pattern underlies the generation of the neural sequences controlling song.

[1]  David Poeppel,et al.  Cortical oscillations and speech processing: emerging computational principles and operations , 2012, Nature Neuroscience.

[2]  M. Fee,et al.  A hypothesis for basal ganglia-dependent reinforcement learning in the songbird , 2011, Neuroscience.

[3]  R. Bertram,et al.  Electrophysiological characterization and computational models of HVC neurons in the zebra finch. , 2013, Journal of neurophysiology.

[4]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[5]  Christopher M. Glaze,et al.  Temporal Structure in Zebra Finch Song: Implications for Motor Coding , 2006, The Journal of Neuroscience.

[6]  Alexander S. Ecker,et al.  Recording chronically from the same neurons in awake, behaving primates. , 2007, Journal of neurophysiology.

[7]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[8]  M. Magnasco,et al.  Simple motor gestures for birdsongs. , 2001, Physical review letters.

[9]  Hugo Merchant,et al.  Interval Tuning in the Primate Medial Premotor Cortex as a General Timing Mechanism , 2013, The Journal of Neuroscience.

[10]  Mengru Li,et al.  Stable propagation of a burst through a one-dimensional homogeneous excitatory chain model of songbird nucleus HVC. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  F. Nottebohm,et al.  Connections of vocal control nuclei in the canary telencephalon , 1982, The Journal of comparative neurology.

[12]  Barbara G. Shinn-Cunningham,et al.  Sparse Contour Representations of Sound , 2012, IEEE Signal Processing Letters.

[13]  Lacey J. Kitch,et al.  Long-term dynamics of CA1 hippocampal place codes , 2013, Nature Neuroscience.

[14]  Timothy J. Gardner,et al.  The Song Must Go On: Resilience of the Songbird Vocal Motor Pathway , 2012, PloS one.

[15]  A. Georgopoulos,et al.  Mapping of the preferred direction in the motor cortex , 2007, Proceedings of the National Academy of Sciences.

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

[17]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[18]  Richard Hans Robert Hahnloser,et al.  Activity in a Premotor Cortical Nucleus of Zebra Finches Is Locally Organized and Exhibits Auditory Selectivity in Neurons but Not in Glia , 2013, PloS one.

[19]  Ramon Bartolo,et al.  Dynamic Representation of the Temporal and Sequential Structure of Rhythmic Movements in the Primate Medial Premotor Cortex , 2014, The Journal of Neuroscience.

[20]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[21]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

[22]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

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

[24]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[25]  B. B. Scott,et al.  Generation of tissue-specific transgenic birds with lentiviral vectors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  N. Hatsopoulos,et al.  Propagating waves mediate information transfer in the motor cortex , 2006, Nature Neuroscience.

[27]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[28]  György Buzsáki,et al.  Erratum: Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo (Nature (2003) 421, (844-848)) , 2006 .

[29]  Simon X. Chen,et al.  Emergence of reproducible spatiotemporal activity during motor learning , 2014, Nature.

[30]  Hugo Merchant,et al.  Information Processing in the Primate Basal Ganglia during Sensory-Guided and Internally Driven Rhythmic Tapping , 2014, The Journal of Neuroscience.

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

[32]  D. Tank,et al.  Functional Clustering of Neurons in Motor Cortex Determined by Cellular Resolution Imaging in Awake Behaving Mice , 2009, The Journal of Neuroscience.

[33]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  T. Nick,et al.  Rhythmic cortical neurons increase their oscillations and sculpt basal ganglia signaling during motor learning , 2013, Developmental neurobiology.

[35]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[36]  Haruo Kasai,et al.  Spatiotemporal Dynamics of Functional Clusters of Neurons in the Mouse Motor Cortex during a Voluntary Movement , 2013, The Journal of Neuroscience.

[37]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[38]  Timothy J. Gardner,et al.  Long-range Order in Canary Song , 2013, PLoS Comput. Biol..

[39]  Mark J. Basista,et al.  Axial Organization of a Brain Region That Sequences a Learned Pattern of Behavior , 2012, The Journal of Neuroscience.

[40]  R. Mooney.  Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch , 2000, The Journal of Neuroscience.

[41]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[42]  Michale S Fee,et al.  Wandering Neuronal Migration in the Postnatal Vertebrate Forebrain , 2012, The Journal of Neuroscience.

[43]  Kyle L. Terleski,et al.  Directed functional connectivity matures with motor learning in a cortical pattern generator. , 2013, Journal of neurophysiology.

[44]  Manuel Guizar-Sicairos,et al.  Efficient subpixel image registration algorithms. , 2008, Optics letters.

[45]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[46]  Marc F. Schmidt,et al.  Pattern of interhemispheric synchronization in HVc during singing correlates with key transitions in the song pattern. , 2003, Journal of neurophysiology.

[47]  Richard S. J. Frackowiak,et al.  Endogenous Cortical Rhythms Determine Cerebral Specialization for Speech Perception and Production , 2007, Neuron.

[48]  Asohan Amarasingham,et al.  Hippocampus Internally Generated Cell Assembly Sequences in the Rat , 2011 .

[49]  Naoya Aoki,et al.  Developmental modulation of the temporal relationship between brain and behavior. , 2007, Journal of neurophysiology.

[50]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

[51]  A. Gamal,et al.  Miniaturized integration of a fluorescence microscope , 2011, Nature Methods.

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

[53]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[54]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[55]  K. D. Punta,et al.  An ultra-sparse code underlies the generation of neural sequences in a songbird , 2002 .

[56]  Richard A. Andersen,et al.  Latent variable models for neural data analysis , 1999 .

[57]  William A Liberti,et al.  A carbon-fiber electrode array for long-term neural recording , 2013, Journal of neural engineering.

[58]  Thomas Naselaris,et al.  Large-scale organization of preferred directions in the motor cortex. II. Analysis of local distributions. , 2006, Journal of neurophysiology.

[59]  R. Mooney,et al.  The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways , 2005, The Journal of Neuroscience.

[60]  R. Bertram,et al.  Two neural streams, one voice: Pathways for theme and variation in the songbird brain , 2014, Neuroscience.

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