Perturbing Neural Representations of Working Memory with Task-irrelevant Interruption

Working memory maintains information so that it can be used in complex cognitive tasks. A key challenge for this system is to maintain relevant information in the face of task-irrelevant perturbations. Across two experiments, we investigated the impact of task-irrelevant interruptions on neural representations of working memory. We recorded EEG activity in humans while they performed a working memory task. On a subset of trials, we interrupted participants with salient but task-irrelevant objects. To track the impact of these task-irrelevant interruptions on neural representations of working memory, we measured two well-characterized, temporally sensitive EEG markers that reflect active, prioritized working memory representations: the contralateral delay activity and lateralized alpha power (8–12 Hz). After interruption, we found that contralateral delay activity amplitude momentarily sustained but was gone by the end of the trial. Lateralized alpha power was immediately influenced by the interrupters but recovered by the end of the trial. This suggests that dissociable neural processes contribute to the maintenance of working memory information and that brief irrelevant onsets disrupt two distinct online aspects of working memory. In addition, we found that task expectancy modulated the timing and magnitude of how these two neural signals responded to task-irrelevant interruptions, suggesting that the brain's response to task-irrelevant interruption is shaped by task context.

[1]  Edward K. Vogel,et al.  Contralateral Delay Activity Tracks Fluctuations in Working Memory Performance , 2018, Journal of Cognitive Neuroscience.

[2]  H. Müller,et al.  Attentional capture by salient color singleton distractors is modulated by top-down dimensional set. , 2009, Journal of experimental psychology. Human perception and performance.

[3]  Geoffrey F. Woodman,et al.  The cost of accessing an object's feature stored in visual working memory , 2011, Visual cognition.

[4]  Keisuke Fukuda,et al.  Distinct neural mechanisms for spatially lateralized and spatially global visual working memory representations. , 2016, Journal of neurophysiology.

[5]  I. A. Clark,et al.  Attention Restores Discrete Items to Visual Short-Term Memory , 2013, Psychological science.

[6]  Raj M. Ratwani,et al.  Recovering from Interruptions: Does Alert Type Matter? , 2009 .

[7]  M. Chun,et al.  Interactions between attention and memory , 2007, Current Opinion in Neurobiology.

[8]  James W Bisley,et al.  Activity of neurons in cortical area MT during a memory for motion task. , 2004, Journal of neurophysiology.

[9]  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.

[10]  R. Dell’Acqua,et al.  The Demonstration of Short-Term Consolidation , 1998, Cognitive Psychology.

[11]  John M. Gaspar,et al.  Suppression of Salient Objects Prevents Distraction in Visual Search , 2014, The Journal of Neuroscience.

[12]  Jarrod A. Lewis-Peacock,et al.  Behavioral decoding of working memory items inside and outside the focus of attention , 2018, Annals of the New York Academy of Sciences.

[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]  Roger W Remington,et al.  Unexpected abrupt onsets can override a top-down set for color. , 2015, Journal of experimental psychology. Human perception and performance.

[15]  Adam Gazzaley,et al.  Mechanisms of working memory disruption by external interference. , 2010, Cerebral cortex.

[16]  E. Vogel,et al.  Visual short-term memory capacity predicts the “bandwidth” of visual long-term memory encoding , 2019, Memory & Cognition.

[17]  Leonardo Chelazzi,et al.  The costly filtering of potential distraction: evidence for a supramodal mechanism. , 2013, Journal of experimental psychology. General.

[18]  Nicole Hakim,et al.  Dissecting the Neural Focus of Attention Reveals Distinct Processes for Spatial Attention and Object-Based Storage in Visual Working Memory , 2018, bioRxiv.

[19]  Edward K Vogel,et al.  Neural Evidence for the Contribution of Active Suppression During Working Memory Filtering , 2019, Cerebral cortex.

[20]  Christian N L Olivers,et al.  Interactions between visual working memory and visual attention. , 2008, Frontiers in bioscience : a journal and virtual library.

[21]  Thomas Töllner,et al.  Top-down dimensional weight set determines the capture of visual attention: evidence from the PCN component. , 2012, Cerebral cortex.

[22]  B. Postle,et al.  Effects of verbal and nonverbal interference on spatial and object visual working memory , 2005, Memory & cognition.

[23]  Edward K. Vogel,et al.  The Contribution of Attentional Lapses to Individual Differences in Visual Working Memory Capacity , 2015, Journal of Cognitive Neuroscience.

[24]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

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

[26]  Melonie Williams,et al.  Directed forgetting and directed remembering in visual working memory. , 2012, Journal of experimental psychology. Learning, memory, and cognition.

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

[28]  Anna Schubö,et al.  Context homogeneity facilitates both distractor inhibition and target enhancement. , 2013, Journal of vision.

[29]  Edward Awh,et al.  Spatially Selective Alpha Oscillations Reveal Moment-by-Moment Trade-offs between Working Memory and Attention , 2018, Journal of Cognitive Neuroscience.

[30]  G. Horstmann Attentional capture by an unannounced color singleton depends on expectation discrepancy. , 2005, Journal of experimental psychology. Human perception and performance.

[31]  Edward Awh,et al.  Contralateral Delay Activity Indexes Working Memory Storage, Not the Current Focus of Spatial Attention , 2018, Journal of Cognitive Neuroscience.

[32]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

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

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

[35]  G. Woodman,et al.  The role of working memory and long-term memory in visual search , 2006 .

[36]  Edward Awh,et al.  Alpha-Band Activity Reveals Spontaneous Representations of Spatial Position in Visual Working Memory , 2017, Current Biology.

[37]  G. Woodman,et al.  The time course of consolidation in visual working memory. , 2006, Journal of experimental psychology. Human perception and performance.

[38]  Edward Awh,et al.  Alpha-Band Activity Revea ls Spontaneous Representations of Spatial Position in VisualWorking Memory Highlights , 2017 .

[39]  Edward Awh,et al.  The contralateral delay activity as a neural measure of visual working memory , 2016, Neuroscience & Biobehavioral Reviews.

[40]  Steven J Luck,et al.  Active suppression of distractors that match the contents of visual working memory , 2011, Visual cognition.

[41]  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.

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