Comparing the Effects of 10-Hz Repetitive TMS on Tasks of Visual STM and Attention

Numerous studies have demonstrated that visual STM (VSTM) and attention are tightly linked processes that share a number of neuroanatomical substrates. Here, we used repetitive TMS (rTMS) along with simultaneous EEG to examine the causal relationship between intraparietal sulcus functioning and performance on tasks of attention and VSTM. Participants performed two tasks in which they were required to attend to or remember colored items over a brief interval, with 10-Hz rTMS applied on some of the trials. Although no overall behavioral changes were observed across either task, rTMS did affect individual performance on both the attention and VSTM tasks in a manner that was predicted by individual differences in baseline performance. Furthermore, rTMS also affected ongoing oscillations in the alpha and beta bands, and these changes were related to the observed change in behavioral performance. The results reveal a causal relationship between intraparietal sulcus activity and tasks measuring both visual attention and VSTM.

[1]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

[2]  R. J. Ilmoniemi,et al.  Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation , 1999, Medical & Biological Engineering & Computing.

[3]  B. Postle.  Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[4]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[5]  J. Wolfe,et al.  Using Fmri to Distinguish Components of the Multiple Object Tracking Task , 1994 .

[6]  J. Theeuwes,et al.  Remembering a Location Makes the Eyes Curve Away , 2005, Psychological science.

[7]  Geraint Rees,et al.  Stochastic Resonance Effects Reveal the Neural Mechanisms of Transcranial Magnetic Stimulation , 2011, The Journal of Neuroscience.

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

[9]  B. Postle.  Neural Bases of the Short-term Retention of Visual Information , 2016 .

[10]  Nicolas Robitaille,et al.  Distinguishing between lateralized and nonlateralized brain activity associated with visual short-term memory: fMRI, MEG, and EEG evidence from the same observers , 2010, NeuroImage.

[11]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[12]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[13]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[14]  Edward F. Ester,et al.  Parietal and Frontal Cortex Encode Stimulus-Specific Mnemonic Representations during Visual Working Memory , 2015, Neuron.

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

[16]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[17]  Barry D. Van Veen,et al.  Context-specific differences in fronto-parieto-occipital effective connectivity during short-term memory maintenance , 2015, NeuroImage.

[18]  Steven J. Luck,et al.  ERPLAB: an open-source toolbox for the analysis of event-related potentials , 2014, Front. Hum. Neurosci..

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

[20]  Giulio Tononi,et al.  Brain responses evoked by high-frequency repetitive transcranial magnetic stimulation: An event-related potential study , 2010, Brain Stimulation.

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

[22]  L. Chanes,et al.  Arrhythmic activity in the left frontal eye field facilitates conscious visual perception in humans , 2015, Cortex.

[23]  Alexa B. Roggeveen,et al.  Large-scale gamma-band phase synchronization and selective attention. , 2008, Cerebral cortex.

[24]  Paul M Bays,et al.  Dynamic Shifts of Limited Working Memory Resources in Human Vision , 2008, Science.

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

[26]  Jason B Mattingley,et al.  Distributed and Overlapping Neural Substrates for Object Individuation and Identification in Visual Short-Term Memory. , 2014, Cerebral cortex.

[27]  Daniel J. Mitchell,et al.  Flexible, capacity-limited activity of posterior parietal cortex in perceptual as well as visual short-term memory tasks. , 2008, Cerebral cortex.

[28]  M. Stokes.  ‘Activity-silent’ working memory in prefrontal cortex: a dynamic coding framework , 2015, Trends in Cognitive Sciences.

[29]  Bradley R. Postle,et al.  Decoding and Reconstructing the Focus of Spatial Attention from the Topography of Alpha-band Oscillations , 2016, Journal of Cognitive Neuroscience.

[30]  Jeffrey S. Johnson,et al.  Trait-like Differences in Underlying Oscillatory State Predict Individual Differences in the TMS-evoked Response , 2014, Brain Stimulation.

[31]  W. Klimesch,et al.  'Paradoxical' alpha synchronization in a memory task. , 1999, Brain research. Cognitive brain research.

[32]  Adam C. Riggall,et al.  Distributed Patterns of Activity in Sensory Cortex Reflect the Precision of Multiple Items Maintained in Visual Short-Term Memory , 2013, The Journal of Neuroscience.

[33]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[34]  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.

[35]  Jeffrey S. Johnson,et al.  Using EEG to Explore How rTMS Produces Its Effects on Behavior , 2009, Brain Topography.

[36]  Daniel J. Mitchell,et al.  Human Neuroscience , 2022 .

[37]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

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

[39]  John-Dylan Haynes,et al.  Decoding the Contents of Visual Short-Term Memory from Human Visual and Parietal Cortex , 2012, The Journal of Neuroscience.

[40]  Jarrod A. Lewis-Peacock,et al.  Multiple neural states of representation in short-term memory? It’s a matter of attention , 2014, Front. Hum. Neurosci..

[41]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

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

[43]  David Melcher,et al.  A Shared, Flexible Neural Map Architecture Reflects Capacity Limits in Both Visual Short-Term Memory and Enumeration , 2014, The Journal of Neuroscience.

[44]  David W. Sutterer,et al.  The topography of alpha-band activity tracks the content of spatial working memory. , 2016, Journal of neurophysiology.

[45]  John J. Foxe,et al.  Anticipatory Attentional Suppression of Visual Features Indexed by Oscillatory Alpha-Band Power Increases:A High-Density Electrical Mapping Study , 2010, The Journal of Neuroscience.

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

[47]  Adam C. Riggall,et al.  The Relationship between Working Memory Storage and Elevated Activity as Measured with Functional Magnetic Resonance Imaging , 2012, The Journal of Neuroscience.

[48]  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.

[49]  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.

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

[51]  Keisuke Fukuda,et al.  α Power Modulation and Event-Related Slow Wave Provide Dissociable Correlates of Visual Working Memory , 2015, The Journal of Neuroscience.

[52]  Kimron Shapiro,et al.  Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Daniel J. Acheson,et al.  Increased Alpha-Band Power during the Retention of Shapes and Shape-Location Associations in Visual Short-Term Memory , 2011, Front. Psychology.

[54]  John-Dylan Haynes,et al.  Decoding complex flow-field patterns in visual working memory , 2014, NeuroImage.

[55]  T. Egner,et al.  Working memory as internal attention: Toward an integrative account of internal and external selection processes , 2012, Psychonomic Bulletin & Review.

[56]  E. Vogel,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[57]  E. Vogel,et al.  Neural Limits to Representing Objects Still within View , 2013, The Journal of Neuroscience.

[58]  Jeffrey S. Johnson,et al.  Task-dependent changes in cortical excitability and effective connectivity: a combined TMS-EEG study. , 2012, Journal of neurophysiology.

[59]  A. Treisman,et al.  Attentional demands predict short-term memory load response in posterior parietal cortex , 2009, Neuropsychologia.

[60]  R. Marois,et al.  Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity , 2005, Cognitive, affective & behavioral neuroscience.

[61]  Nicolas Robitaille,et al.  Oscillatory activity in parietal and dorsolateral prefrontal cortex during retention in visual short‐term memory: Additive effects of spatial attention and memory load , 2009, Human brain mapping.

[62]  M. Massimini,et al.  Natural Frequencies of Human Corticothalamic Circuits , 2009, The Journal of Neuroscience.

[63]  P. Downing,et al.  Mapping brain activation and information during category-specific visual working memory. , 2012, Journal of neurophysiology.

[64]  P. Jolicoeur,et al.  Bilateral parietal and contralateral responses during maintenance of unilaterally encoded objects in visual short-term memory: evidence from magnetoencephalography. , 2009, Psychophysiology.