Prefrontal high gamma during a magnetoencephalographic working memory task

In human electrophysiology research, the high gamma part of the power spectrum (~>60 Hz) is a relatively new area of investigation. Despite a low signal‐to‐noise ratio, evidence exists that it contains significant information about activity in local cortical networks. Here, using magnetoencephalography (MEG), we found high gamma activity when comparing data from an n‐back working memory task to resting data in a large sample of normal volunteers. Initial analysis of power spectra from 0‐back, 2‐back, and rest trials showed three frequency bands exhibiting task‐related differences: alpha, beta, and high gamma. Unlike alpha and beta, the high gamma spectrum was broad, without a peak at a single frequency. In addition, power in high gamma was highest for the 2‐back and lowest during rest, while the opposite pattern occurred in the other bands. Beamformer source localization of each of the three frequency bands revealed a distinct set of sources for high gamma. These included several regions of prefrontal cortex that exhibited greater power when both n‐back conditions were compared to rest. A subset of these regions had more power when the 2‐back was compared to 0‐back, which indicates a role in working memory performance. Our results show that high gamma will be important for understanding cortical processing during cognitive and other tasks. Furthermore, data from human intracortical recordings suggest that high gamma is the aggregate of spiking in local cortical networks, which implies that MEG could serve to bridge experimental modalities by noninvasively observing task‐related modulation of spiking rates.

[1]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[2]  Brent M. Berry,et al.  Dissecting gamma frequency activity during human memory processing , 2017, Brain : a journal of neurology.

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

[4]  Roland R. Lee,et al.  MEG Working Memory N-Back Task Reveals Functional Deficits in Combat-Related Mild Traumatic Brain Injury. , 2019, Cerebral cortex.

[5]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[6]  Matthew J. Brookes,et al.  Optimising experimental design for MEG beamformer imaging , 2008, NeuroImage.

[7]  P. Goldman-Rakic.  The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  A. Altamura,et al.  Assessing Working Memory via N-Back Task in Euthymic Bipolar I Disorder Patients: A Review of Functional Magnetic Resonance Imaging Studies , 2013, Neuropsychobiology.

[9]  H. Berger.  Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

[10]  E. Basar,et al.  Gamma-band responses in the brain: a short review of psychophysiological correlates and functional significance. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[12]  René Scheeringa,et al.  The relationship between oscillatory EEG activity and the laminar-specific BOLD signal , 2016, Proceedings of the National Academy of Sciences.

[13]  Edward T. Bullmore,et al.  Reproducibility of graph metrics of human brain functional networks , 2009, NeuroImage.

[14]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[15]  Tony W. Wilson,et al.  Spatiotemporal oscillatory dynamics during the encoding and maintenance phases of a visual working memory task , 2015, Cortex.

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

[17]  György Buzsáki,et al.  High frequency oscillations in the intact brain , 2012, Progress in Neurobiology.

[18]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[19]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[20]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[21]  Peter F. Liddle,et al.  Changes in brain network activity during working memory tasks: A magnetoencephalography study , 2011, NeuroImage.

[22]  Walter Paulus,et al.  Noninvasively Decoding the Contents of Visual Working Memory in the Human Prefrontal Cortex within High-gamma Oscillatory Patterns , 2012, Journal of Cognitive Neuroscience.

[23]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[24]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[25]  N. Crone,et al.  Afferent inputs to cortical fast-spiking interneurons organize pyramidal cell network oscillations at high-gamma frequencies (60-200 Hz). , 2014, Journal of Neurophysiology.

[26]  Wolf Singer,et al.  Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia , 2013, Front. Hum. Neurosci..

[27]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[28]  Nicole M. Long,et al.  Subsequent memory effect in intracranial and scalp EEG , 2014, NeuroImage.

[29]  R. Coppola,et al.  Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. , 2000, Cerebral cortex.

[30]  Paul Ferrari,et al.  Self-paced movements induce high-frequency gamma oscillations in primary motor cortex , 2008, NeuroImage.

[31]  Nicole M. Long,et al.  Human intracranial high-frequency activity maps episodic memory formation in space and time , 2014, NeuroImage.

[32]  Rajesh P. N. Rao,et al.  Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations , 2014, NeuroImage.

[33]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[34]  Luke Bloy,et al.  Evidence for a motor gamma-band network governing response interference , 2013, NeuroImage.

[35]  J. Cohen,et al.  Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. , 2001, The American journal of psychiatry.

[36]  Paul Ferrari,et al.  MEG studies of motor cortex gamma oscillations: evidence for a gamma “fingerprint” in the brain? , 2013, Front. Hum. Neurosci..

[37]  M Schürmann,et al.  Functional aspects of alpha oscillations in the EEG. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  N. Crone,et al.  Cortical γ responses: searching high and low. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  Margot J. Taylor,et al.  Atypical spatiotemporal signatures of working memory brain processes in autism , 2015, Translational Psychiatry.

[40]  Paul Ferrari,et al.  Complementary roles of cortical oscillations in automatic and controlled processing during rapid serial tasks , 2015, NeuroImage.

[41]  J. R. Hughes,et al.  RESPONSES FROM THE VISUAL CORTEX OF UNANESTHETIZED MONKEYS. , 1964, International review of neurobiology.

[42]  F. D. Silva,et al.  EEG and MEG: Relevance to Neuroscience , 2013, Neuron.

[43]  William Gaetz,et al.  Neuromagnetic imaging of movement-related cortical oscillations in children and adults: Age predicts post-movement beta rebound , 2010, NeuroImage.

[44]  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.

[45]  Tom Holroyd,et al.  Anterior Cingulate Desynchronization and Functional Connectivity with the Amygdala During a Working Memory Task Predict Rapid Antidepressant Response to Ketamine , 2010, Neuropsychopharmacology.

[46]  K. Miller.  Broadband Spectral Change: Evidence for a Macroscale Correlate of Population Firing Rate? , 2010, The Journal of Neuroscience.

[47]  M. Furey,et al.  Baseline working memory activation deficits in dimensional anxious depression as detected by magnetoencephalography , 2015, Acta Neuropsychiatrica.

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

[49]  R. Straub,et al.  Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[50]  B. Levine,et al.  Treating Working Memory Deficits in Schizophrenia: A Review of the Neurobiology , 2014, Biological Psychiatry.

[51]  Richard C. Reynolds,et al.  SUMA , 2012, NeuroImage.

[52]  Wilkin Chau,et al.  An integrative MEG–fMRI study of the primary somatosensory cortex using cross-modal correspondence analysis , 2004, NeuroImage.

[53]  Richard Coppola,et al.  Prefrontal Cortex Modulation during Anticipation of Working Memory Demands as Revealed by Magnetoencephalography , 2010, Int. J. Biomed. Imaging.

[54]  Michael J Kahana,et al.  Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? , 2015, Current Opinion in Neurobiology.

[55]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique , 2001, IEEE Transactions on Biomedical Engineering.

[56]  Yusuke Suzuki,et al.  The inhibition/excitation ratio related to task-induced oscillatory modulations during a working memory task: A multtimodal-imaging study using MEG and MRS , 2016, NeuroImage.

[57]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[58]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[59]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

[60]  L. Bartova,et al.  Reduced default mode network suppression during a working memory task in remitted major depression , 2015, Journal of psychiatric research.

[61]  Wolf Singer,et al.  High-frequency oscillations and the neurobiology of schizophrenia , 2013, Dialogues in clinical neuroscience.

[62]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

[63]  J. Wallis,et al.  The Role of Prefrontal Cortex in Working Memory: A Mini Review , 2015, Front. Syst. Neurosci..

[64]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[65]  Michael A. DiSano,et al.  Variability of the Relationship between Electrophysiology and BOLD-fMRI across Cortical Regions in Humans , 2011, The Journal of Neuroscience.

[66]  E. Bedrick,et al.  Top-down control of MEG alpha-band activity in children performing Categorical N-Back Task , 2010, Neuropsychologia.

[67]  Rajesh P. N. Rao,et al.  High gamma mapping using EEG , 2010, NeuroImage.

[68]  S Makeig,et al.  Human auditory evoked gamma-band magnetic fields. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Andreas Schulze-Bonhage,et al.  Movement related activity in the high gamma range of the human EEG , 2008, NeuroImage.

[70]  A. Arnsten.  Stress signalling pathways that impair prefrontal cortex structure and function , 2009, Nature Reviews Neuroscience.

[71]  L. Selemon,et al.  Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder , 2001, Biological Psychiatry.

[72]  E. Chang,et al.  UC San Francisco UC San Francisco Previously Published Works Title Oscillatory dynamics coordinating human frontal networks in support of goal maintenance , 2015 .

[73]  E. Martin,et al.  Simultaneous EEG-fMRI during a Working Memory Task: Modulations in Low and High Frequency Bands , 2010, PloS one.

[74]  F. H. Lopes da Silva.  EEG and MEG: relevance to neuroscience. , 2013, Neuron.

[75]  W. Freeman,et al.  Frequency analysis of olfactory system EEG in cat, rabbit, and rat. , 1980, Electroencephalography and clinical neurophysiology.