Double dissociation of working memory load effects induced by bilateral parietal modulation

Transcranial magnetic stimulation and neuroimaging data have revealed bilateral posterior parietal cortex (PPC) involvement during verbal n-back working memory (WM). In this task as n (i.e., WM load) increases, subjects show poorer behavioral performance as well as greater activation of this brain area. Moreover, there is evidence that a brief period of practice or even increased familiarity with the task can improve WM performance and lead to activation changes in the PPC. The aim of this study was to investigate, using transcranial direct current stimulation (tDCS), the effects on WM load performance induced by different PPC modulation after increased familiarity with the task. After a short practice, we tested verbal WM using an n-back task (1-back vs. 2-back) before and after the application of bilateral tDCS over PPCs (left anodal-right cathodal, left cathodal-right anodal or sham). ANOVA showed a significant interaction between tDCS and task. In the 1-back task, left anodal-right cathodal modulation abolished improvement in reaction times observed in the other two modulation conditions. Conversely, in the 2-back task the same effect was observed after left cathodal-right anodal modulation relative to the other two modulation conditions. This double dissociation demonstrates either a differential engagement of each PPC or changes in the interhemispheric balance of activity across this brain region. Neuroimaging studies show parametric activation of the PPC as difficulty increases, but activation does not switch sides. Thus, our observed effects cannot be attributed to increased task difficulty, the stimuli used, or the response requirements. Rather, we suggest that these findings reflect the use of different processing strategies to perform these two tasks. In conclusion, after increased familiarity with the task, different tDCS modulations lead to changes in a task-related region depending on differences in processing strategies in 1-back vs. 2-back.

[1]  Elizabeth A. Kensinger,et al.  What Neural Correlates Underlie Successful Encoding and Retrieval? A Functional Magnetic Resonance Imaging Study Using a Divided Attention Paradigm , 2003, The Journal of Neuroscience.

[2]  Sara Torriero,et al.  rTMS evidence of different delay and decision processes in a fronto-parietal neuronal network activated during spatial working memory , 2005, NeuroImage.

[3]  Sergio P. Rigonatti,et al.  Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory , 2005, Experimental Brain Research.

[4]  P. Enticott,et al.  Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex , 2011, Brain Stimulation.

[5]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[6]  M. Just,et al.  From the SelectedWorks of Marcel Adam Just 1992 A capacity theory of comprehension : Individual differences in working memory , 2017 .

[7]  John E. Desmond,et al.  Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study , 2005, NeuroImage.

[8]  Charan Ranganath,et al.  Effects of Unilateral Prefrontal Lesions on Familiarity, Recollection, and Source Memory , 2005, The Journal of Neuroscience.

[9]  Marsha C. Lovett,et al.  A source activation theory of working memory: cross-task prediction of performance in ACT-R , 2000, Cognitive Systems Research.

[10]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[11]  Robin M. Chan,et al.  Working memory for complex figures: an fMRI comparison of letter and fractal n-back tasks. , 2002, Neuropsychology.

[12]  B. Postle,et al.  Superior Parietal Cortex Is Critical for the Manipulation of Information in Working Memory , 2009, The Journal of Neuroscience.

[13]  Hugh Garavan,et al.  Practice‐related functional activation changes in a working memory task , 2000, Microscopy research and technique.

[14]  Clayton E. Curtis,et al.  Behavioral and neurophysiological correlates of episodic coding, proactive interference, and list length effects in a running span verbal working memory task , 2001, Cognitive, affective & behavioral neuroscience.

[15]  C. Degueldre,et al.  Regional brain activity during working memory tasks. , 1996, Brain : a journal of neurology.

[16]  A. Baddeley.  The episodic buffer: a new component of working memory? , 2000, Trends in Cognitive Sciences.

[17]  A. Baddeley.  Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[18]  Anusha Venkatakrishnan,et al.  Combining transcranial direct current stimulation and neuroimaging: novel insights in understanding neuroplasticity. , 2012, Journal of neurophysiology.

[19]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[20]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

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

[22]  Marcia K. Johnson,et al.  Prefrontal Cortex Activity Associated with Source Monitoring in a Working Memory Task , 2004, Journal of Cognitive Neuroscience.

[23]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[24]  Felix M Mottaghy,et al.  Modulation of a brain-behavior relationship in verbal working memory by rTMS. , 2003, Brain research. Cognitive brain research.

[25]  Valerie Kirsch,et al.  Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: A standardized low resolution tomography (sLORETA) study , 2011, NeuroImage.

[26]  Stefan Elmer,et al.  Behavioral and Brain Functions , 2009 .

[27]  Richard J. Brown.  Neuropsychology Mental Structure , 1989 .

[28]  Giulio Tononi,et al.  Repetitive Transcranial Magnetic Stimulation Dissociates Working Memory Manipulation from Retention Functions in the Prefrontal, but not Posterior Parietal, Cortex , 2006, Journal of Cognitive Neuroscience.

[29]  A. Antal,et al.  Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients , 2007, Brain Research Bulletin.

[30]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[32]  Felix M Mottaghy,et al.  Bilateral parieto‐frontal network for verbal working memory: an interference approach using repetitive transcranial magnetic stimulation (rTMS) , 2002, The European journal of neuroscience.

[33]  Serge A. R. B. Rombouts,et al.  Practice effects in the brain: Changes in cerebral activation after working memory practice depend on task demands , 2010, NeuroImage.

[34]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[35]  Jan Born,et al.  Bifrontal transcranial direct current stimulation slows reaction time in a working memory task , 2005, BMC Neuroscience.

[36]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[37]  P. Rossini,et al.  Consensus paper: Combining transcranial stimulation with neuroimaging , 2009, Brain Stimulation.

[38]  J. Fiez,et al.  Using neuroimaging to evaluate models of working memory and their implications for language processing , 2003, Journal of Neurolinguistics.

[39]  Alfredo Brancucci,et al.  Effects of Transcranial Direct Current Stimulation on Episodic Memory Related to Emotional Visual Stimuli , 2010, PloS one.

[40]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  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.

[43]  A. Yonelinas.  The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[44]  Maro G. Machizawa,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[45]  Kaia L. Vilberg,et al.  Functional significance of retrieval‐related activity in lateral parietal cortex: Evidence from fMRI and ERPs , 2009, Human brain mapping.

[46]  G. Tononi,et al.  Evaluating frontal and parietal contributions to spatial working memory with repetitive transcranial magnetic stimulation , 2008, Brain Research.

[47]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

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

[49]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[50]  M. Hogge,et al.  Exploration of the neural substrates of executive functioning by functional neuroimaging , 2006, Neuroscience.

[51]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[52]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  Daniel L. Schacter,et al.  fMRI Evidence for Separable and Lateralized Prefrontal Memory Monitoring Processes , 2004, Journal of Cognitive Neuroscience.

[54]  Jieun Kim,et al.  Effects of Verbal Working Memory Load on Corticocortical Connectivity Modeled by Path Analysis of Functional Magnetic Resonance Imaging Data , 2002, NeuroImage.

[55]  H J Tochon-Danguy,et al.  Updating working memory for words: A PET activation study , 2000, Human brain mapping.

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

[57]  M Gangitano,et al.  Chronometry of parietal and prefrontal activations in verbal working memory revealed by transcranial magnetic stimulation , 2003, NeuroImage.

[58]  A. Gevins,et al.  Spatiotemporal dynamics of component processes in human working memory. , 1993, Electroencephalography and clinical neurophysiology.

[59]  Kaia L. Vilberg,et al.  Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective , 2008, Neuropsychologia.

[60]  Uwe Herwig,et al.  Using the International 10-20 EEG System for Positioning of Transcranial Magnetic Stimulation , 2004, Brain Topography.

[61]  A. Miyake,et al.  Models of Working Memory: Mechanisms of Active Maintenance and Executive Control , 1999 .

[62]  Felipe Fregni,et al.  Visual memory improved by non-invasive brain stimulation , 2010, Brain Research.

[63]  R. Knight,et al.  Dissociable neural correlates for familiarity and recollection during the encoding and retrieval of pictures. , 2004, Brain research. Cognitive brain research.

[64]  V. Walsh,et al.  Modulating Neuronal Activity Produces Specific and Long-Lasting Changes in Numerical Competence , 2010, Current Biology.

[65]  Y. Kim,et al.  Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory , 2008, Neuroreport.

[66]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[67]  V. Walsh,et al.  Transcranial Direct Current Stimulation Facilitates Decision Making in a Probabilistic Guessing Task , 2010, The Journal of Neuroscience.

[68]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[69]  Stephan Heckers,et al.  Hemispheric specialization of the lateral prefrontal cortex for strategic processing during spatial and shape working memory , 2004, NeuroImage.

[70]  Bradley R. Buchsbaum,et al.  The Search for the Phonological Store: From Loop to Convolution , 2008, Journal of Cognitive Neuroscience.

[71]  David Badre,et al.  Frontal lobe mechanisms that resolve proactive interference. , 2005, Cerebral cortex.

[72]  Walter Paulus,et al.  Transcranial direct current stimulation over the primary motor cortex during fMRI , 2011, NeuroImage.

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

[74]  Edward T. Bullmore,et al.  Prolonged Reaction Time to a Verbal Working Memory Task Predicts Increased Power of Posterior Parietal Cortical Activation , 2000, NeuroImage.

[75]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[76]  Á. Pascual-Leone,et al.  Activation of Prefrontal Cortex by Transcranial Direct Current Stimulation Reduces Appetite for Risk during Ambiguous Decision Making , 2007, The Journal of Neuroscience.

[77]  Á. Pascual-Leone,et al.  Modulation of decision‐making in a gambling task in older adults with transcranial direct current stimulation , 2010, The European journal of neuroscience.

[78]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[79]  Jonathan D. Cohen,et al.  Working Memory for Letters, Shapes, and Locations: fMRI Evidence against Stimulus-Based Regional Organization in Human Prefrontal Cortex , 2000, NeuroImage.

[80]  Edward E. Smith,et al.  Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET , 1997, Journal of Cognitive Neuroscience.

[81]  Richard S. J. Frackowiak,et al.  How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? , 2005, The European journal of neuroscience.

[82]  Myra A. Fernandes,et al.  Neural correlates of recollection and familiarity: A review of neuroimaging and patient data , 2007, Neuropsychologia.

[83]  J. Isaiah Harbison,et al.  N-back Training Task Performance: Analysis and Model , 2011, CogSci.

[84]  Sara Marceglia,et al.  Cerebellar Transcranial Direct Current Stimulation Impairs the Practice-dependent Proficiency Increase in Working Memory , 2008, Journal of Cognitive Neuroscience.

[85]  A. Priori.  Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability , 2003, Clinical Neurophysiology.

[86]  F. M. Mottaghy,et al.  Interfering with working memory in humans , 2006, Neuroscience.

[87]  Alvaro Pascual-Leone,et al.  Temporal Lobe Cortical Electrical Stimulation during the Encoding and Retrieval Phase Reduces False Memories , 2009, PloS one.

[88]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

[89]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[90]  Gottfried Schlaug,et al.  Dual-hemisphere tDCS facilitates greater improvements for healthy subjects' non-dominant hand compared to uni-hemisphere stimulation , 2008, BMC Neuroscience.