TMS-induced neural noise in sensory cortex interferes with short-term memory storage in prefrontal cortex

In a previous study, Harris et al. (2002) found disruption of vibrotactile short-term memory after applying single-pulse transcranial magnetic stimulation (TMS) to primary somatosensory cortex (SI) early in the maintenance period, and suggested that this demonstrated a role for SI in vibrotactile memory storage. While such a role is compatible with recent suggestions that sensory cortex is the storage substrate for working memory, it stands in contrast to a relatively large body of evidence from human EEG and single-cell recording in primates that instead points to prefrontal cortex as the storage substrate for vibrotactile memory. In the present study, we use computational methods to demonstrate how Harris et al.'s results can be reproduced by TMS-induced activity in sensory cortex and subsequent feedforward interference with memory traces stored in prefrontal cortex, thereby reconciling discordant findings in the tactile memory literature.

[1]  Felix Blankenburg,et al.  Supramodal Parametric Working Memory Processing in Humans , 2012, The Journal of Neuroscience.

[2]  Felix Blankenburg,et al.  Working memory coding of analog stimulus properties in the human prefrontal cortex. , 2014, Cerebral cortex.

[3]  B. Meyer,et al.  Evaluation of cortical excitability by motor and phosphene thresholds in transcranial magnetic stimulation , 2003, Journal of the Neurological Sciences.

[4]  A. Pascual-Leone,et al.  Studies in Cognition: The Problems Solved and Created by Transcranial Magnetic Stimulation , 2003, Journal of Cognitive Neuroscience.

[5]  Facilitation of tactile working memory by top-down suppression from prefrontal to primary somatosensory cortex during sensory interference , 2011, Behavioural Brain Research.

[6]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[7]  M. Sugishita,et al.  Paraesthesia elicited by repetitive magnetic stimulation of the postcentral gyrus. , 1993, Neuroreport.

[8]  Hartwig R. Siebner,et al.  BOLD MRI responses to repetitive TMS over human dorsal premotor cortex , 2005, NeuroImage.

[9]  R. Oostenveld,et al.  Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network , 2009, Human brain mapping.

[10]  Patrick Ragert,et al.  Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex , 2007, Experimental Brain Research.

[11]  Tomás Paus,et al.  Inferring causality in brain images: a perturbation approach , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  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.

[13]  Klaus Funke,et al.  Effect of transcranial magnetic stimulation on single‐unit activity in the cat primary visual cortex , 2003, The Journal of physiology.

[14]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[15]  M. Ptito,et al.  TMS of the occipital cortex induces tactile sensations in the fingers of blind Braille readers , 2007, Experimental Brain Research.

[16]  Colin W G Clifford,et al.  Improving Visual Sensitivity with Subthreshold Transcranial Magnetic Stimulation , 2011, The Journal of Neuroscience.

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

[18]  Felix Blankenburg,et al.  Stimulus-dependent EEG activity reflects internal updating of tactile working memory in humans , 2011, Proceedings of the National Academy of Sciences.

[19]  William E. Hockley,et al.  Vibrotactile Working Memory as a Model Paradigm for Psychology, Neuroscience, and Computational Modeling , 2011, Front. Hum. Neurosci..

[20]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[22]  Patrick Ragert,et al.  Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans , 2004, Neuroscience Letters.

[23]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[24]  J. Rothwell,et al.  Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study , 2001, Neuropsychologia.

[25]  Justin A. Harris,et al.  The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression or Neural Noise Generation? , 2008, Journal of Cognitive Neuroscience.

[26]  Paul Miller,et al.  Inhibitory control by an integral feedback signal in prefrontal cortex: a model of discrimination between sequential stimuli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Petri Savolainen,et al.  Increasing top-down suppression from prefrontal cortex facilitates tactile working memory , 2010, NeuroImage.

[28]  Antonio P Strafella,et al.  Transcranial magnetic stimulation of the human motor cortex influences the neuronal activity of subthalamic nucleus , 2004, The European journal of neuroscience.

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

[30]  Mechanisms of Interference in Vibrotactile Working Memory , 2011, PloS one.

[31]  C M Epstein,et al.  Magnetic stimulation of visual cortex: factors influencing the perception of phosphenes. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[32]  Tyler D. Bancroft,et al.  Does stimulus complexity determine whether working memory storage relies on prefrontal or sensory cortex? , 2014, Attention, perception & psychophysics.

[33]  Ziad Nahas,et al.  A combined TMS/fMRI study of intensity-dependent TMS over motor cortex , 1999, Biological Psychiatry.

[34]  Tyler D. Bancroft,et al.  Distractor frequency influences performance in vibrotactile working memory , 2011, Experimental Brain Research.

[35]  F. Blankenburg,et al.  Recurrent Neural Processing and Somatosensory Awareness , 2012, The Journal of Neuroscience.

[36]  P M Rossini,et al.  Paired transcranial magnetic stimulation protocols reveal a pattern of inhibition and facilitation in the human parietal cortex , 2000, The Journal of physiology.

[37]  Tyler D. Bancroft,et al.  Diffusion modeling of interference in vibrotactile working memory , 2012, Neuroreport.

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

[39]  Neil G. Muggleton,et al.  New light through old windows: Moving beyond the “virtual lesion” approach to transcranial magnetic stimulation , 2008, NeuroImage.

[40]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

[41]  Tyler D. Bancroft,et al.  Irrelevant sensory stimuli interfere with working memory storage: Evidence from a computational model of prefrontal neurons , 2013, Cognitive, affective & behavioral neuroscience.

[42]  Saskia Haegens,et al.  Somatosensory Anticipatory Alpha Activity Increases to Suppress Distracting Input , 2012, Journal of Cognitive Neuroscience.

[43]  G B Arden,et al.  The Visual System , 2021, AMA Guides to the Evaluation of Permanent Impairment, 6th Edition, 2021.

[44]  Felix Blankenburg,et al.  Oscillatory Correlates of Vibrotactile Frequency Processing in Human Working Memory , 2010, The Journal of Neuroscience.

[45]  Brian N. Pasley,et al.  State-Dependent Variability of Neuronal Responses to Transcranial Magnetic Stimulation of the Visual Cortex , 2009, Neuron.

[46]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[47]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.