The strength of alpha and gamma oscillations predicts behavioral switch costs

ABSTRACT Cognitive flexibility is often examined using task‐switch paradigms, whereby individuals either switch between tasks or repeat the same task on successive trials. The behavioral costs of switching in terms of accuracy and reaction time are well‐known, but the oscillatory dynamics underlying such costs are poorly understood. Herein, we examined 25 healthy adults who performed a task‐switching paradigm during magnetoencephalography (MEG). All MEG data were transformed into the time‐frequency domain and significant oscillatory responses were imaged separately per condition (i.e., switch, repeat) using a beamformer. To determine the impact of task‐switching on the neural dynamics, the resulting images were examined using paired‐samples t‐tests. Whole‐brain correlations were also computed using the switch‐related difference images (switch – repeat) and the switch‐related behavioral data (i.e., switch costs). Our key results indicated stronger decreases in alpha and beta activity, and greater increases in gamma activity in nodes of the cingulo‐opercular and fronto‐parietal networks during switch relative to repeat trials. In addition, behavioral switch costs were positively correlated with switch‐related differences in right frontal and inferior parietal alpha activity, and negatively correlated with switch effects in anterior cingulate and right temporoparietal gamma activity. In other words, participants who had a greater decrease in alpha or increase in gamma in these respective regions had smaller behavioral switch costs, which suggests that these oscillations are critical to supporting cognitive flexibility. In sum, we provide novel data linking switch effects and gamma oscillations, and employed a whole‐brain approach to directly link switch‐related oscillatory differences with switch‐related performance differences. HIGHLIGHTSTask‐switching costs are well known, but their oscillatory signature is unclear.Adults performed a task‐switching paradigm during magnetoencephalography (MEG).MEG data were subjected to a beamformer and advanced oscillatory analysis methods.Task‐switching distinctly modulated behavior, alpha, beta, and gamma oscillations.Switch effects on alpha and gamma oscillations were tied to behavioral switch costs.

[1]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[2]  M. D. Ernst Permutation Methods: A Basis for Exact Inference , 2004 .

[3]  E. Crone,et al.  Neural evidence for dissociable components of task-switching. , 2006, Cerebral cortex.

[4]  L. Lemieux,et al.  Electrophysiological correlates of the BOLD signal for EEG‐informed fMRI , 2014, Human brain mapping.

[5]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[6]  Maximilian Reiser,et al.  Single-trial coupling of the gamma-band response and the corresponding BOLD signal , 2010, NeuroImage.

[7]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[8]  M. Brass,et al.  Involvement of the inferior frontal junction in cognitive control: Meta‐analyses of switching and Stroop studies , 2005, Human brain mapping.

[9]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[10]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[11]  Alan C. Evans,et al.  Detecting changes in nonisotropic images , 1999, Human brain mapping.

[12]  André Knops,et al.  Numerical ordering and symbolic arithmetic share frontal and parietal circuits in the right hemisphere , 2014, NeuroImage.

[13]  J. Schoffelen,et al.  Oscillatory activity in human parietal and occipital cortex shows hemispheric lateralization and memory effects in a delayed double-step saccade task. , 2007, Cerebral cortex.

[14]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

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

[16]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[17]  C. Carter,et al.  Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Patrick S. Cooper,et al.  Frontoparietal theta oscillations during proactive control are associated with goal-updating and reduced behavioral variability , 2017, Biological Psychology.

[19]  Ritske de Jong,et al.  Pre-stimulus EEG effects related to response speed, task switching and upcoming response hand , 2006, Biological Psychology.

[20]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[21]  Karl J. Friston,et al.  Estimating Smoothness in Statistical Parametric Maps: Variability of p Values , 1995, Journal of computer assisted tomography.

[22]  Jonathan D. Cohen,et al.  Between-Task Competition and Cognitive Control in Task Switching , 2006, The Journal of Neuroscience.

[23]  Christian Beste,et al.  On the relevance of the alpha frequency oscillation’s small-world network architecture for cognitive flexibility , 2017, Scientific Reports.

[24]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[25]  Jed A. Meltzer,et al.  Individual differences in EEG theta and alpha dynamics during working memory correlate with fMRI responses across subjects , 2007, Clinical Neurophysiology.

[26]  N. Cohen,et al.  General and task-specific frontal lobe recruitment in older adults during executive processes: A fMRI investigation of task-switching , 2001, Neuroreport.

[27]  A. Allport,et al.  Task switching and the measurement of “switch costs” , 2000, Psychological research.

[28]  John R. Anderson,et al.  The role of prefrontal cortex and posterior parietal cortex in task switching. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[30]  Amy L. Proskovec,et al.  Neuroimaging with magnetoencephalography: A dynamic view of brain pathophysiology. , 2016, Translational research : the journal of laboratory and clinical medicine.

[31]  John J. Foxe,et al.  Neuro-oscillatory mechanisms of intersensory selective attention and task switching in school-aged children, adolescents and young adults. , 2016, Developmental science.

[32]  Nick Yeung,et al.  Dissociable Neural Correlates of Intention and Action Preparation in Voluntary Task Switching , 2012, Cerebral cortex.

[33]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[34]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[35]  K. Amunts,et al.  Posterior parietal cortex is implicated in continuous switching between verbal fluency tasks: an fMRI study with clinical implications , 2002 .

[36]  A. Dove,et al.  Prefrontal cortex activation in task switching: an event-related fMRI study. , 2000, Brain research. Cognitive brain research.

[37]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[38]  A. Anastasi Individual differences. , 2020, Annual review of psychology.

[39]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.

[40]  Wim Fias,et al.  Common and distinct brain regions in both parietal and frontal cortex support symbolic and nonsymbolic number processing in humans: A functional neuroimaging meta-analysis , 2017, NeuroImage.

[41]  Francisco Barceló,et al.  Contextually sensitive power changes across multiple frequency bands underpin cognitive control , 2016, NeuroImage.

[42]  Alex I. Wiesman,et al.  Oscillatory dynamics in the dorsal and ventral attention networks during the reorienting of attention , 2018, Human brain mapping.

[43]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[44]  Antao Chen,et al.  The neural dynamic mechanisms of asymmetric switch costs in a combined Stroop-task-switching paradigm , 2015, Scientific Reports.

[45]  R. Ilmoniemi,et al.  Signal-space projection method for separating MEG or EEG into components , 1997, Medical and Biological Engineering and Computing.

[46]  G. D. Logan Task Switching , 2022 .

[47]  Alex I. Wiesman,et al.  Spatiotemporal oscillatory dynamics of visual selective attention during a flanker task , 2017, NeuroImage.

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

[49]  Tony W Wilson,et al.  Aging modulates the oscillatory dynamics underlying successful working memory encoding and maintenance , 2016, Human brain mapping.

[50]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[51]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[52]  Margot J. Taylor,et al.  Neuromagnetic correlates of intra- and extra-dimensional set-shifting , 2014, Brain and Cognition.

[53]  S. Monsell,et al.  Costs of a predictible switch between simple cognitive tasks. , 1995 .

[54]  Cameron S Carter,et al.  Gamma Oscillatory Power is Impaired During Cognitive Control Independent of Medication Status in First-Episode Schizophrenia , 2010, Neuropsychopharmacology.

[55]  John J. Foxe,et al.  Throwing out the rules: anticipatory alpha‐band oscillatory attention mechanisms during task‐set reconfigurations , 2014, The European journal of neuroscience.

[56]  B. Gold,et al.  Domain general and domain preferential brain regions associated with different types of task switching: A Meta‐Analysis , 2012, Human brain mapping.

[57]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[58]  Xiaochun Wang,et al.  Neural correlates of interference resolution in the multi-source interference task: a meta-analysis of functional neuroimaging studies , 2018, Behavioral and Brain Functions.

[59]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[60]  Raymond Cluydts,et al.  Attentional switching‐related human EEG alpha oscillations , 2002, Neuroreport.

[61]  D Brandeis,et al.  Simultaneous EEG-fMRI during a working memory task: Distinct modulations of lower and higher EEG frequencies , 2009, NeuroImage.

[62]  Scott Makeig,et al.  Brain oscillations in switching vs. focusing audio-visual attention , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[63]  N. Meiran,et al.  Component Processes in Task Switching , 2000, Cognitive Psychology.

[64]  Robert Oostenveld,et al.  Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance , 2009, NeuroImage.

[65]  Jordan Grafman,et al.  The Roles of Timing and Task Order during Task Switching , 2002, NeuroImage.

[66]  W. Klimesch,et al.  Relevance of EEG alpha and theta oscillations during task switching , 2006, Experimental Brain Research.

[67]  H H Donaldson,et al.  LOCALIZATION IN THE BRAIN. , 1884, Science.

[68]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[69]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[70]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[71]  C. Carter,et al.  Impairments in frontal cortical γ synchrony and cognitive control in schizophrenia , 2006, Proceedings of the National Academy of Sciences.

[72]  Antoni Rodríguez-Fornells,et al.  Brain oscillatory activity associated with task switching and feedback processing , 2011, Cognitive, Affective, & Behavioral Neuroscience.

[73]  R. Jong,et al.  Bursts of occipital theta and alpha amplitude preceding alternation and repetition trials in a task-switching experiment , 2005, Biological Psychology.