Multiple foci of spatial attention in multimodal working memory

The maintenance of sensory information in working memory (WM) is mediated by the attentional activation of stimulus representations that are stored in perceptual brain regions. Using event-related potentials (ERPs), we measured tactile and visual contralateral delay activity (tCDA/CDA components) in a bimodal WM task to concurrently track the attention-based maintenance of information stored in anatomically segregated (somatosensory and visual) brain areas. Participants received tactile and visual sample stimuli on both sides, and in different blocks, memorized these samples on the same side or on opposite sides. After a retention delay, memory was unpredictably tested for touch or vision. In the same side blocks, tCDA and CDA components simultaneously emerged over the same hemisphere, contralateral to the memorized tactile/visual sample set. In opposite side blocks, these two components emerged over different hemispheres, but had the same sizes and onset latencies as in the same side condition. Our results reveal distinct foci of tactile and visual spatial attention that were concurrently maintained on task-relevant stimulus representations in WM. The independence of spatially-specific biasing mechanisms for tactile and visual WM content suggests that multimodal information is stored in distributed perceptual brain areas that are activated through modality-specific processes that can operate simultaneously and largely independently of each other.

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

[2]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[3]  J Driver,et al.  An event-related brain potential study of cross-modal links in spatial attention between vision and touch. , 2000, Psychophysiology.

[4]  Terrence J. Sejnowski,et al.  Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis , 2007, NeuroImage.

[5]  A. Engel,et al.  Tactile remapping: from coordinate transformation to integration in sensorimotor processing , 2015, Trends in Cognitive Sciences.

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

[7]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[8]  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.

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

[10]  P. Cavanagh,et al.  Flexible cognitive resources: competitive content maps for attention and memory , 2013, Trends in Cognitive Sciences.

[11]  Jeffrey N. Rouder,et al.  Default Bayes factors for ANOVA designs , 2012 .

[12]  P. Haggard,et al.  The Posterior Parietal Cortex Remaps Touch into External Space , 2010, Current Biology.

[13]  E. Vogel,et al.  Contralateral delay activity provides a neural measure of the number of representations in visual working memory. , 2010, Journal of neurophysiology.

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

[15]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[16]  Emilio Salinas,et al.  Cognitive neuroscience: Flutter Discrimination: neural codes, perception, memory and decision making , 2003, Nature Reviews Neuroscience.

[17]  A. Pouget,et al.  Reference frames for representing visual and tactile locations in parietal cortex , 2005, Nature Neuroscience.

[18]  A. Nobre,et al.  Cognitive control of attention in the human brain: Insights from orienting attention to mental representations , 2006, Brain Research.

[19]  Hiroshi Handa,et al.  A Neural Correlate of Working Memory in the Monkey Primary Visual Cortex , 2017 .

[20]  R. B. Reilly,et al.  FASTER: Fully Automated Statistical Thresholding for EEG artifact Rejection , 2010, Journal of Neuroscience Methods.

[21]  Maria V. Sanchez-Vives,et al.  Hyperpolarization-activated graded persistent activity in the prefrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[22]  E. Wagenmakers,et al.  Bayesian hypothesis testing for psychologists: A tutorial on the Savage–Dickey method , 2010, Cognitive Psychology.

[23]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

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

[25]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[26]  W Pieter Medendorp,et al.  Parietofrontal circuits in goal‐oriented behaviour , 2011, The European journal of neuroscience.

[27]  J. Driver,et al.  Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies , 2001, Neuroscience & Biobehavioral Reviews.

[28]  Nancy Kanwisher,et al.  Retinotopic memory is more precise than spatiotopic memory , 2012, Proceedings of the National Academy of Sciences.

[29]  Kartik K. Sreenivasan,et al.  Revisiting the role of persistent neural activity during working memory , 2014, Trends in Cognitive Sciences.

[30]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

[31]  M. R. Riley,et al.  Role of Prefrontal Persistent Activity in Working Memory , 2016, Front. Syst. Neurosci..

[32]  E. Schröger,et al.  ERP effects of intermodal attention and cross-modal links in spatial attention. , 1998, Psychophysiology.

[33]  Jöran Lepsien,et al.  Searching for Targets within the Spatial Layout of Visual Short-Term Memory , 2009, The Journal of Neuroscience.

[34]  J. Driver,et al.  Audiovisual links in endogenous covert spatial attention. , 1996, Journal of experimental psychology. Human perception and performance.

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

[36]  J. Driver,et al.  Cross-modal links in endogenous spatial attention are mediated by common external locations: evidence from event-related brain potentials , 2001, Experimental Brain Research.

[37]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[38]  Martin Eimer,et al.  Lateralized Delay Period Activity Marks the Focus of Spatial Attention in Working Memory: Evidence from Somatosensory Event-Related Brain Potentials , 2015, The Journal of Neuroscience.

[39]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[40]  Martin Eimer,et al.  Electrophysiological Evidence for a Sensory Recruitment Model of Somatosensory Working Memory. , 2015, Cerebral cortex.

[41]  H. Barbas Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[42]  Edward K. Vogel,et al.  Shape and color conjunction stimuli are represented as bound objects in visual working memory , 2011 .

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

[44]  L. M. M.-T. Theory of Probability , 1929, Nature.

[45]  Jeff Miller,et al.  Jackknife-based method for measuring LRP onset latency differences. , 1998, Psychophysiology.

[46]  Julio C. Martinez-Trujillo,et al.  Sharp emergence of feature-selective sustained activity along the dorsal visual pathway , 2014, Nature Neuroscience.

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

[48]  C. Curtis,et al.  Common neural mechanisms supporting spatial working memory, attention and motor intention , 2011, Neuropsychologia.

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

[50]  Jeff Miller,et al.  Using the jackknife-based scoring method for measuring LRP onset effects in factorial designs. , 2001, Psychophysiology.

[51]  P. Cavanagh,et al.  Visual stability based on remapping of attention pointers , 2010, Trends in Cognitive Sciences.

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

[53]  Matthias M. Müller,et al.  Working memory delay period activity marks a domain-unspecific attention mechanism , 2016, NeuroImage.

[54]  C. Spence,et al.  Crossmodal links between vision and touch in covert endogenous spatial attention. , 2000, Journal of experimental psychology. Human perception and performance.

[55]  N. Cowan The focus of attention as observed in visual working memory tasks: Making sense of competing claims , 2011, Neuropsychologia.

[56]  Julie D. Golomb,et al.  The Native Coordinate System of Spatial Attention Is Retinotopic , 2008, The Journal of Neuroscience.

[57]  C. Tenke,et al.  Generator localization by current source density (CSD): Implications of volume conduction and field closure at intracranial and scalp resolutions , 2012, Clinical Neurophysiology.

[58]  Nelson Cowan,et al.  A Neural Region of Abstract Working Memory , 2011, Journal of Cognitive Neuroscience.

[59]  S. Kastner,et al.  Topographic maps in human frontal and parietal cortex , 2009, Trends in Cognitive Sciences.

[60]  E. Vogel,et al.  Shape and color conjunction stimuli are represented as bound objects in visual working memory , 2011, Neuropsychologia.

[61]  John Jonides,et al.  Processes of Working Memory in Mind and Brain , 2005 .

[62]  Martin Eimer,et al.  Crossmodal links in spatial attention between vision, audition, and touch: evidence from event-related brain potentials , 2001, Neuropsychologia.

[63]  C. Spence,et al.  Attention and the crossmodal construction of space , 1998, Trends in Cognitive Sciences.

[64]  E. Vogel,et al.  Interactions between attention and working memory , 2006, Neuroscience.

[65]  Clayton E. Curtis,et al.  Maps of space in human frontoparietal cortex , 2013, Journal of Physiology-Paris.

[66]  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.

[67]  J. Fellous,et al.  Intrinsic subthreshold oscillations extend the influence of inhibitory synaptic inputs on cortical pyramidal neurons , 2010, The European journal of neuroscience.

[68]  Søren K. Andersen,et al.  Nonspatial Cueing of Tactile STM Causes Shift of Spatial Attention , 2012, Journal of Cognitive Neuroscience.

[69]  Matthias M. Müller,et al.  Sustained Maintenance of Somatotopic Information in Brain Regions Recruited by Tactile Working Memory , 2015, The Journal of Neuroscience.