Task-Dependent Changes in Cross-Level Coupling between Single Neurons and Oscillatory Activity in Multiscale Networks

Understanding the principles governing the dynamic coordination of functional brain networks remains an important unmet goal within neuroscience. How do distributed ensembles of neurons transiently coordinate their activity across a variety of spatial and temporal scales? While a complete mechanistic account of this process remains elusive, evidence suggests that neuronal oscillations may play a key role in this process, with different rhythms influencing both local computation and long-range communication. To investigate this question, we recorded multiple single unit and local field potential (LFP) activity from microelectrode arrays implanted bilaterally in macaque motor areas. Monkeys performed a delayed center-out reach task either manually using their natural arm (Manual Control, MC) or under direct neural control through a brain-machine interface (Brain Control, BC). In accord with prior work, we found that the spiking activity of individual neurons is coupled to multiple aspects of the ongoing motor beta rhythm (10–45 Hz) during both MC and BC, with neurons exhibiting a diversity of coupling preferences. However, here we show that for identified single neurons, this beta-to-rate mapping can change in a reversible and task-dependent way. For example, as beta power increases, a given neuron may increase spiking during MC but decrease spiking during BC, or exhibit a reversible shift in the preferred phase of firing. The within-task stability of coupling, combined with the reversible cross-task changes in coupling, suggest that task-dependent changes in the beta-to-rate mapping play a role in the transient functional reorganization of neural ensembles. We characterize the range of task-dependent changes in the mapping from beta amplitude, phase, and inter-hemispheric phase differences to the spike rates of an ensemble of simultaneously-recorded neurons, and discuss the potential implications that dynamic remapping from oscillatory activity to spike rate and timing may hold for models of computation and communication in distributed functional brain networks.

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

[2]  Maureen A. Hagan,et al.  Only Coherent Spiking in Posterior Parietal Cortex Coordinates Looking and Reaching , 2012, Neuron.

[3]  D. Poeppel,et al.  Auditory Cortex Tracks Both Auditory and Visual Stimulus Dynamics Using Low-Frequency Neuronal Phase Modulation , 2010, PLoS biology.

[4]  B. Staresina,et al.  Medial Temporal Theta/Alpha Power Enhancement Precedes Successful Memory Encoding: Evidence Based on Intracranial EEG , 2011, The Journal of Neuroscience.

[5]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[6]  S. Bressler.  Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[7]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[8]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[9]  Matthias Bethge,et al.  Statistical Analysis of Multi-Cell Recordings: Linking Population Coding Models to Experimental Data , 2011, Front. Comput. Neurosci..

[10]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

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

[12]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[13]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[14]  N. Hatsopoulos,et al.  Periodicity and Evoked Responses in Motor Cortex , 2010, The Journal of Neuroscience.

[15]  H. S. Meyer,et al.  Cell Type–Specific Three-Dimensional Structure of Thalamocortical Circuits in a Column of Rat Vibrissal Cortex , 2011, Cerebral cortex.

[16]  Karl J. Friston,et al.  Forward and backward connections in the brain: A DCM study of functional asymmetries , 2009, NeuroImage.

[17]  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.

[18]  Nick F. Ramsey,et al.  Human Motor Cortical Activity Is Selectively Phase-Entrained on Underlying Rhythms , 2012, PLoS Comput. Biol..

[19]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[20]  D. W. Wheeler,et al.  Behavioral performance modulates spike field coherence in monkey prefrontal cortex , 2008, Neuroreport.

[21]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Xiao-Jing Wang.  Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[23]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[24]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[25]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A. Graybiel,et al.  Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum , 2011, Proceedings of the National Academy of Sciences.

[27]  Anders Lansner,et al.  Bistable, Irregular Firing and Population Oscillations in a Modular Attractor Memory Network , 2010, PLoS Comput. Biol..

[28]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[29]  N. Hatsopoulos,et al.  Propagating Waves in Human Motor Cortex , 2011, Front. Hum. Neurosci..

[30]  Idan Segev,et al.  Optimization principles of dendritic structure , 2007, Theoretical Biology and Medical Modelling.

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

[32]  L. Scharf,et al.  Statistical Signal Processing of Complex-Valued Data: The Theory of Improper and Noncircular Signals , 2010 .

[33]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[34]  Marcelo A. Montemurro,et al.  Spike-Phase Coding Boosts and Stabilizes Information Carried by Spatial and Temporal Spike Patterns , 2009, Neuron.

[35]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[36]  W. Singer,et al.  Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle , 2012, Proceedings of the National Academy of Sciences.

[37]  Yoram Ben-Shaul,et al.  Temporally precise cortical firing patterns are associated with distinct action segments. , 2006, Journal of neurophysiology.

[38]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[39]  W. Singer,et al.  Synchrony Makes Neurons Fire in Sequence, and Stimulus Properties Determine Who Is Ahead , 2011, The Journal of Neuroscience.

[40]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[41]  G. Edelman,et al.  Spike-timing dynamics of neuronal groups. , 2004, Cerebral cortex.

[42]  Bagrat Amirikian,et al.  Directional tuning profiles of motor cortical cells , 2000, Neuroscience Research.

[43]  Botond Szatmáry,et al.  Spike-Timing Theory of Working Memory , 2010, PLoS Comput. Biol..

[44]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[45]  R. Romo,et al.  Beta oscillations in the monkey sensorimotor network reflect somatosensory decision making , 2011, Proceedings of the National Academy of Sciences.

[46]  E. M. Pinches,et al.  The role of synchrony and oscillations in the motor output , 1999, Experimental Brain Research.

[47]  Stuart N Baker,et al.  Afferent encoding of central oscillations in the monkey arm. , 2006, Journal of neurophysiology.

[48]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[49]  J. Donoghue,et al.  Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. , 1998, Journal of neurophysiology.

[50]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[51]  Miles A. Whittington,et al.  Human Neuroscience , 2022 .

[52]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[53]  David Eriksson,et al.  A Linear Model of Phase-Dependent Power Correlations in Neuronal Oscillations , 2011, Front. Comput. Neurosci..

[54]  J. Carmena,et al.  Emergence of a Stable Cortical Map for Neuroprosthetic Control , 2009, PLoS biology.

[55]  Karl J. Friston.  Hierarchical Models in the Brain , 2008, PLoS Comput. Biol..

[56]  Kevan A. C. Martin,et al.  Canonical cortical circuits , 2010 .

[57]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[58]  J. Palva,et al.  Neuronal synchrony reveals working memory networks and predicts individual memory capacity , 2010, Proceedings of the National Academy of Sciences.

[59]  Peter Lakatos,et al.  Dynamics of Active Sensing and perceptual selection , 2010, Current Opinion in Neurobiology.

[60]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[61]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[62]  M. Siegel,et al.  A framework for local cortical oscillation patterns , 2011, Trends in Cognitive Sciences.

[63]  E. Fetz,et al.  Synaptic interactions mediating synchrony and oscillations in primate sensorimotor cortex , 2000, Journal of Physiology-Paris.

[64]  Stuart N Baker,et al.  Manipulation of peripheral neural feedback loops alters human corticomuscular coherence , 2005, The Journal of physiology.

[65]  Gustavo Deco,et al.  Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme , 2009, The Journal of Neuroscience.

[66]  Bijan Pesaran,et al.  Spike-field activity in parietal area LIP during coordinated reach and saccade movements , 2011, Journal of neurophysiology.

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

[68]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

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

[70]  Miles A Whittington,et al.  A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex , 2006, Proceedings of the National Academy of Sciences.

[71]  S. Baker.  Oscillatory interactions between sensorimotor cortex and the periphery , 2007, Current Opinion in Neurobiology.

[72]  G. Shepherd,et al.  Geometric and functional organization of cortical circuits , 2005, Nature Neuroscience.

[73]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[74]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[75]  N. Hatsopoulos,et al.  Fast and Slow Oscillations in Human Primary Motor Cortex Predict Oncoming Behaviorally Relevant Cues , 2010, Neuron.

[76]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

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

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

[79]  K. Koepsell,et al.  Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies , 2010, Proceedings of the National Academy of Sciences.

[80]  Karl J. Friston.  The free-energy principle: a rough guide to the brain? , 2009, Trends in Cognitive Sciences.

[81]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[82]  Masataka Watanabe,et al.  Human Neuroscience Original Research Article Awareness of Central Luminance Edge Is Crucial for the Craik-o'brien-cornsweet Effect , 2022 .

[83]  O. Paulsen,et al.  Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information , 2008, The Journal of physiology.