Transcranial direct current stimulation over right posterior parietal cortex changes prestimulus alpha oscillation in visual short-term memory task

Alpha band activity changes accompanied with the level attentional state, and recent studies suggest that such oscillation is associated with activities in the posterior parietal cortex. Here we show that artificially elevating parietal activity via positively-charged electric current through the skull can rapidly and effortlessly change people's prestimulus alpha power and improve subsequent performance on a visual short-term memory (VSTM) task. This modulation of alpha power and behavioral performance, however, is dependent on people's natural VSTM capability such that only the low performers benefitted from the stimulation, whereas high performers did not. This behavioral dichotomy is accounted by prestimulus alpha powers around the parieto-occipital regions: low performers showed decreased prestimulus alpha power, suggesting improvement in attention deployment in the current paradigm, whereas the high performers did not benefit from tDCS as they showed equally-low prestimulus alpha power before and after the stimulation. Together, these results suggest that prestimulus alpha power, especially in low performers, can be modulated by anodal stimulation and alter subsequent VSTM performance/capacity. Thus, measuring alpha before stimulus onset may be as important as measuring other VSTM-related electrophysiological components such as attentional allocation and memory capacity related components (i.e. N2 posterior-contralateral, N2pc, or contralateral delay activity, CDA). In addition, low VSTM performers perhaps do not suffer not only from poor VSTM capacity, but also from broad attentional mechanisms, and prestimulus alpha may be an useful tool in understanding the nature of individual differences in VSTM.

[1]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

[2]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[3]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[4]  E. Vogel,et al.  Quantity, not quality: the relationship between fluid intelligence and working memory capacity , 2010, Psychonomic bulletin & review.

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

[6]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  Neil G. Muggleton,et al.  Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex , 2011, NeuroImage.

[8]  Juha Silvanto,et al.  The causal role of category-specific neuronal representations in the left ventral premotor cortex (PMv) in semantic processing , 2010, NeuroImage.

[9]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[10]  Robert Sekuler,et al.  Attention-modulated Alpha-band Oscillations Protect against Intrusion of Irrelevant Information , 2013, Journal of Cognitive Neuroscience.

[11]  A. Nobre,et al.  Alpha Oscillations Related to Anticipatory Attention Follow Temporal Expectations , 2011, The Journal of Neuroscience.

[12]  W. Medendorp,et al.  Modulations in oscillatory activity with amplitude asymmetry can produce cognitively relevant event-related responses , 2009, Proceedings of the National Academy of Sciences.

[13]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[14]  D. Mathalon,et al.  Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. , 2008, Schizophrenia bulletin.

[15]  O. Tzeng,et al.  Unleashing Potential: Transcranial Direct Current Stimulation over the Right Posterior Parietal Cortex Improves Change Detection in Low-Performing Individuals , 2012, The Journal of Neuroscience.

[16]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[17]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[18]  Alison R. Lane,et al.  Near and far space: Understanding the neural mechanisms of spatial attention , 2013, Human brain mapping.

[19]  Gregor Thut,et al.  Brain activity underlying visual perception and attention as inferred from TMS–EEG: A review , 2012, Brain Stimulation.

[20]  V. Walsh,et al.  State-dependency in brain stimulation studies of perception and cognition , 2008, Trends in Cognitive Sciences.

[21]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[22]  F. Tong,et al.  Decoding reveals the contents of visual working memory in early visual areas , 2009, Nature.

[23]  Edward K. Vogel,et al.  The capacity of visual working memory for features and conjunctions , 1997, Nature.

[24]  Chiara Bozzacchi,et al.  Modulation of spontaneous alpha brain rhythms using low-intensity transcranial direct-current stimulation , 2013, Front. Hum. Neurosci..

[25]  Thomas Schenk,et al.  The Involvement of Posterior Parietal Cortex in Feature and Conjunction Visuomotor Search , 2011, Journal of Cognitive Neuroscience.

[26]  J. Jay Todd,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004, Nature.

[27]  M. Lavidor,et al.  Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation , 2012, Clinical Neurophysiology.

[28]  C. Schroeder,et al.  Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations , 2011, The Journal of Neuroscience.

[29]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[30]  P. Schyns,et al.  Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures , 2011, Current Biology.

[31]  E. Vogel,et al.  Visual working memory capacity: from psychophysics and neurobiology to individual differences , 2013, Trends in Cognitive Sciences.

[32]  Gregor Thut,et al.  Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability , 2008, Neuroreport.

[33]  Jeffrey N. Rouder,et al.  How to measure working memory capacity in the change detection paradigm , 2011, Psychonomic bulletin & review.

[34]  A. Burgess,et al.  Paradox lost? Exploring the role of alpha oscillations during externally vs. internally directed attention and the implications for idling and inhibition hypotheses. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.

[36]  M. Corbetta,et al.  Top-Down Control of Human Visual Cortex by Frontal and Parietal Cortex in Anticipatory Visual Spatial Attention , 2008, The Journal of Neuroscience.

[37]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[38]  Violeta Dimova,et al.  Electrified minds: Transcranial direct current stimulation (tDCS) and Galvanic Vestibular Stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology—A review of current data and future implications , 2010, Neuropsychologia.

[39]  O. Jensen,et al.  Asymmetric Amplitude Modulations of Brain Oscillations Generate Slow Evoked Responses , 2008, The Journal of Neuroscience.

[40]  C. Miniussi,et al.  Combining TMS and EEG Offers New Prospects in Cognitive Neuroscience , 2009, Brain Topography.

[41]  Ethan R. Buch,et al.  Noninvasive brain stimulation: from physiology to network dynamics and back , 2013, Nature Neuroscience.

[42]  Vincent Walsh,et al.  Right parietal cortex plays a critical role in change blindness. , 2006, Cerebral cortex.

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

[44]  Carly J. Leonard,et al.  The relationship between working memory capacity and broad measures of cognitive ability in healthy adults and people with schizophrenia. , 2013, Neuropsychology.

[45]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[46]  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.

[47]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[48]  Mingzhou Ding,et al.  From Prestimulus Alpha Oscillation to Visual-evoked Response: An Inverted-U Function and Its Attentional Modulation , 2011, Journal of Cognitive Neuroscience.

[49]  Gregor Thut,et al.  Prediction of response speed by anticipatory high‐frequency (gamma band) oscillations in the human brain , 2005, Human brain mapping.

[50]  Á. Pascual-Leone,et al.  Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. , 2008, Cerebral cortex.

[51]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[52]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[53]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[54]  Bruce Bridgeman,et al.  Improved change detection with nearby hands , 2011, Experimental Brain Research.

[55]  E. Vogel,et al.  Individual Differences in Recovery Time From Attentional Capture , 2011, Psychological science.

[56]  G. Tononi,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Repetitive Transcranial Magnetic Stimulation Affects Behavior by Biasing Endogenous Cortical Oscillations , 2022 .

[57]  Ronald R. Peeters,et al.  Attentional priorities and access to short-term memory: Parietal interactions , 2012, NeuroImage.

[58]  P. Rossini,et al.  Pre- and poststimulus alpha rhythms are related to conscious visual perception: a high-resolution EEG study. , 2005, Cerebral cortex.

[59]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[60]  Maurizio Corbetta,et al.  Electrophysiological Correlates of Stimulus-driven Reorienting Deficits after Interference with Right Parietal Cortex during a Spatial Attention Task: A TMS-EEG Study , 2012, Journal of Cognitive Neuroscience.

[61]  Debora Brignani,et al.  Combining Transcranial Electrical Stimulation With Electroencephalography , 2012, Clinical EEG and neuroscience.

[62]  Ingrid R. Olson,et al.  A selective working memory impairment after transcranial direct current stimulation to the right parietal lobe , 2010, Neuroscience Letters.

[63]  R. Hari,et al.  Modulation of the Parieto-Occipital Alpha Rhythm during Object Detection , 1997, The Journal of Neuroscience.

[64]  Céline R. Gillebert,et al.  Dissociations between spatial-attentional processes within parietal cortex: insights from hybrid spatial cueing and change detection paradigms , 2013, Front. Hum. Neurosci..

[65]  David Soto,et al.  Causal evidence for subliminal percept-to-memory interference in early visual cortex , 2012, NeuroImage.

[66]  Wolfgang Klimesch,et al.  Alpha Oscillations and Early Stages of Visual Encoding , 2011, Front. Psychology.

[67]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[68]  S. Yantis,et al.  Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex. , 2007, Cerebral cortex.

[69]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[70]  W. Klimesch,et al.  Simultaneous desynchronization and synchronization of different alpha responses in the human electroencephalograph: a neglected paradox? , 2000, Neuroscience Letters.

[71]  K. Linkenkaer-Hansen,et al.  Long-Range Temporal Correlations and Scaling Behavior in Human Brain Oscillations , 2001, The Journal of Neuroscience.

[72]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[73]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[74]  M. Berryhill,et al.  Parietal Contributions to Visual Working Memory Depend on Task Difficulty , 2012, Front. Psychiatry.

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

[76]  Charan Ranganath,et al.  Frontal midline theta oscillations during working memory maintenance and episodic encoding and retrieval , 2014, NeuroImage.

[77]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[78]  O. Tzeng,et al.  Posterior parietal cortex mediates encoding and maintenance processes in change blindness , 2010, Neuropsychologia.

[79]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

[80]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[81]  J. Schoffelen,et al.  Parieto‐occipital sources account for the increase in alpha activity with working memory load , 2007, Human brain mapping.

[82]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.