Neurofeedback Training of Gamma Oscillations in Monkey Primary Visual Cortex.

In humans, neurofeedback (NFB) training has been used extensively and successfully to manipulate brain activity. Feedback signals were derived from EEG, fMRI, MEG, and intracranial recordings and modifications were obtained of the BOLD signal, of the power of oscillatory activity in distinct frequency bands and of single unit activity. The purpose of the present study was to examine whether neuronal activity could also be controlled by NFB in early sensory cortices whose activity is thought to be influenced mainly by sensory input rather than volitional control. We trained 2 macaque monkeys to enhance narrow band gamma oscillations in the primary visual cortex by providing them with an acoustic signal that reflected the power of gamma oscillations in a preselected band and rewarding increases of the feedback signal. Oscillations were assessed from local field potentials recorded with chronically implanted microelectrodes. Both monkeys succeeded to raise gamma activity in the absence of visual stimulation in the selected frequency band and at the site from which the NFB signal was derived. This suggests that top-down signals are not confined to just modulate stimulus induced responses but can actually drive or facilitate the gamma generating microcircuits even in a primary sensory area.

[1]  Juliana Y. Rhee,et al.  Acute off-target effects of neural circuit manipulations , 2015, Nature.

[2]  Danko Nikolić,et al.  Scaled correlation analysis: a better way to compute a cross‐correlogram , 2012, The European journal of neuroscience.

[3]  W. Singer,et al.  Progress in Biophysics and Molecular Biology , 1965 .

[4]  J. O'Doherty,et al.  Direct Instrumental Conditioning of Neural Activity Using Functional Magnetic Resonance Imaging-Derived Reward Feedback , 2007, The Journal of Neuroscience.

[5]  Renee Hoch,et al.  Gamma Rhythms Link Prefrontal Interneuron Dysfunction with Cognitive Inflexibility in Dlx5/6 +/− Mice , 2015, Neuron.

[6]  W. Singer,et al.  Endogenously generated gamma‐band oscillations in early visual cortex: A neurofeedback study , 2018, Human brain mapping.

[7]  Aaron R. Seitz,et al.  Cognitive Neuroscience: Targeting Neuroplasticity with Neural Decoding and Biofeedback , 2013, Current Biology.

[8]  J. Maunsell,et al.  Do gamma oscillations play a role in cerebral cortex? , 2015, Trends in Cognitive Sciences.

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

[10]  Gordon Cheng,et al.  Long-Term Training with a Brain-Machine Interface-Based Gait Protocol Induces Partial Neurological Recovery in Paraplegic Patients , 2016, Scientific Reports.

[11]  E. Fetz Volitional control of neural activity: implications for brain–computer interfaces , 2007, The Journal of physiology.

[12]  Jarrod A. Lewis-Peacock,et al.  Closed-loop brain training: the science of neurofeedback , 2017, Nature Reviews Neuroscience.

[13]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[14]  A. Schwartz,et al.  Behavioral and neural correlates of visuomotor adaptation observed through a brain-computer interface in primary motor cortex. , 2012, Journal of neurophysiology.

[15]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[16]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[17]  Mark R. Bower,et al.  High frequency oscillations are associated with cognitive processing in human recognition memory. , 2014, Brain : a journal of neurology.

[18]  R. Goebel,et al.  fMRI Neurofeedback Training for Increasing Anterior Cingulate Cortex Activation in Adult Attention Deficit Hyperactivity Disorder. An Exploratory Randomized, Single-Blinded Study , 2017, PloS one.

[19]  Takeo Watanabe,et al.  Perceptual Learning Incepted by Decoded fMRI Neurofeedback Without Stimulus Presentation , 2011, Science.

[20]  Partha P. Mitra,et al.  Chronux: A platform for analyzing neural signals , 2010, Journal of Neuroscience Methods.

[21]  Wolf Singer,et al.  Gamma-Band Activity in Human Prefrontal Cortex Codes for the Number of Relevant Items Maintained in Working Memory , 2012, The Journal of Neuroscience.

[22]  Karl Herrup,et al.  Neurons in vulnerable regions of the Alzheimer ' s disease brain display reduced 1 ATM signaling 2 Abbreviated title : Loss of ATM function in Alzheimer ' s disease 3 , 2016 .

[23]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[24]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[25]  Geraint Rees,et al.  What can functional imaging reveal about the role of attention in visual awareness? , 2001, Neuropsychologia.

[26]  A. Ehlis,et al.  NIRS-based neurofeedback training in a virtual reality classroom for children with attention-deficit/hyperactivity disorder: study protocol for a randomized controlled trial , 2017, Trials.

[27]  Margaret F. Carr,et al.  Transient Slow Gamma Synchrony Underlies Hippocampal Memory Replay , 2012, Neuron.

[28]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

[29]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[30]  A. Treisman,et al.  Attentional spread in the statistical processing of visual displays , 2005, Perception & psychophysics.

[31]  P. Uhlhaas,et al.  Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? , 2014, Trends in Cognitive Sciences.

[32]  R. Andersen,et al.  Cognitive Control Signals for Neural Prosthetics , 2004, Science.

[33]  Adrian G Bondy,et al.  Saccadic modulation of stimulus processing in primary visual cortex , 2015, Nature Communications.

[34]  Laura Lee Colgin,et al.  Fast Gamma Rhythms in the Hippocampus Promote Encoding of Novel Object–Place Pairings , 2016, eNeuro.

[35]  Wolf Singer,et al.  Neuronal oscillations: unavoidable and useful? , 2018, The European journal of neuroscience.

[36]  Tirin Moore,et al.  Selective Attention from Voluntary Control of Neurons in Prefrontal Cortex , 2011, Science.

[37]  V. Sohal How Close Are We to Understanding What (if Anything) γ Oscillations Do in Cortical Circuits? , 2016, The Journal of Neuroscience.

[38]  Charles M Gray,et al.  Multichannel micromanipulator and chamber system for recording multineuronal activity in alert, non-human primates. , 2007, Journal of neurophysiology.

[39]  Louise S. Delicato,et al.  Acetylcholine contributes through muscarinic receptors to attentional modulation in V1 , 2008, Nature.

[40]  A. Thiele,et al.  Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner , 2007, Nature Neuroscience.

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

[42]  B. C. Motter Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[43]  T. Egner,et al.  Foundation and Practice of Neurofeedback for the Treatment of Epilepsy , 2006, Applied psychophysiology and biofeedback.

[44]  Fred Wolf,et al.  Flexible information routing by transient synchrony , 2017, Nature Neuroscience.

[45]  D. J. McFarland,et al.  Trained modulation of sensorimotor rhythms can affect reaction time , 2011, Clinical Neurophysiology.

[46]  E. Boyden,et al.  Gamma frequency entrainment attenuates amyloid load and modifies microglia , 2016, Nature.

[47]  W. Singer,et al.  Gamma Responses Correlate with Temporal Expectation in Monkey Primary Visual Cortex , 2011, The Journal of Neuroscience.

[48]  Solaiman Shokur,et al.  A Brain-Machine Interface Enables Bimanual Arm Movements in Monkeys , 2013, Science Translational Medicine.

[49]  Christof Koch,et al.  On-line, voluntary control of human temporal lobe neurons , 2010, Nature.

[50]  J. Maunsell,et al.  Attentional Modulation of Behavioral Performance and Neuronal Responses in Middle Temporal and Ventral Intraparietal Areas of Macaque Monkey , 2002, The Journal of Neuroscience.

[51]  R. Oostenveld,et al.  Finding Gamma , 2008, Neuron.

[52]  B. L. Bird,et al.  Biofeedback training of 40-Hz EEG in humans , 1978, Biofeedback and self-regulation.

[53]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[54]  Aaron C. Koralek,et al.  Volitional Modulation of Primary Visual Cortex Activity Requires the Basal Ganglia , 2018, Neuron.

[55]  S. Epstein,et al.  Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model , 2008, Proceedings of the National Academy of Sciences.

[56]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[57]  K. Deisseroth,et al.  Prefrontal Parvalbumin Neurons in Control of Attention , 2016, Cell.

[58]  Tony W Wilson,et al.  tDCS Modulates Visual Gamma Oscillations and Basal Alpha Activity in Occipital Cortices: Evidence from MEG , 2018, Cerebral cortex.

[59]  Bernhard Hommel,et al.  Enhancing cognitive control through neurofeedback: A role of gamma-band activity in managing episodic retrieval , 2010, NeuroImage.

[60]  E. Miller,et al.  Gamma and Beta Bursts Underlie Working Memory , 2016, Neuron.

[61]  Mikhail A Lebedev,et al.  Stable Ensemble Performance with Single-neuron Variability during Reaching Movements in Primates , 2022 .

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

[63]  Hagai Bergman,et al.  Inducing Gamma Oscillations and Precise Spike Synchrony by Operant Conditioning via Brain-Machine Interface , 2013, Neuron.

[64]  N. Birbaumer,et al.  Brain–computer interfaces for communication and rehabilitation , 2016, Nature Reviews Neurology.

[65]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[66]  C. Gilbert,et al.  Top-down influences on visual processing , 2013, Nature Reviews Neuroscience.

[67]  Geraint Rees,et al.  Improving Visual Perception through Neurofeedback , 2012, The Journal of Neuroscience.

[68]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[69]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[70]  K. Harris,et al.  Cortical state and attention , 2011, Nature Reviews Neuroscience.

[71]  John P. Donoghue,et al.  Connecting cortex to machines: recent advances in brain interfaces , 2002, Nature Neuroscience.

[72]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[73]  Jessica A. Cardin,et al.  Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2 , 2010, Nature Protocols.

[74]  Tobias Egner,et al.  Neurofeedback treatment of epilepsy: from basic rationale to practical application , 2006, Expert review of neurotherapeutics.

[75]  Andrew S. Whitford,et al.  Cortical control of a prosthetic arm for self-feeding , 2008, Nature.

[76]  P H Schiller,et al.  Visual representations during saccadic eye movements. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[77]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[78]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

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

[80]  Leonardo Chelazzi,et al.  Neural basis of visual selective attention. , 2011, Wiley interdisciplinary reviews. Cognitive science.

[81]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[82]  Bijan Pesaran,et al.  Parsing learning in networks using brain–machine interfaces , 2017, Current Opinion in Neurobiology.

[83]  E. Fetz Operant Conditioning of Cortical Unit Activity , 1969, Science.

[84]  E. Fetz,et al.  Operant Conditioning of Specific Patterns of Neural and Muscular Activity , 1971, Science.

[85]  T. Egner,et al.  The effect of training distinct neurofeedback protocols on aspects of cognitive performance. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.