Flexibility of representational states in working memory

The relationship between working memory (WM) and attention is a highly interdependent one, with evidence that attention determines the state in which items in WM are retained. Through focusing of attention, an item might be held in a more prioritized state, commonly termed as the focus of attention (FOA). The remaining items, although still retrievable, are considered to be in a different representational state. One means to bring an item into the FOA is to use retrospective cues (“retro-cues”) which direct attention to one of the objects retained in WM. Alternatively, an item can enter a privileged state once attention is directed towards it through bottom-up influences (e.g., recency effect) or by performing an action on one of the retained items (“incidental” cueing). In all these cases, the item in the FOA is recalled with better accuracy compared to the other items in WM. Far less is known about the nature of the other items in WM and whether they can be flexibly manipulated in and out of the FOA. We present data from three types of experiments as well as transcranial magnetic stimulation (TMS) to early visual cortex to manipulate the item inside FOA. Taken together, our results suggest that the context in which items are retained in WM matters. When an item remains behaviorally relevant, despite not being inside the FOA, re-focusing attention upon it can increase its recall precision. This suggests that a non-FOA item can be held in a state in which it can be later retrieved. However, if an item is rendered behaviorally unimportant because it is very unlikely to be probed, it cannot be brought back into the FOA, nor recalled with high precision. Under such conditions, some information appears to be irretrievably lost from WM. These findings, obtained from several different methods, demonstrate quite considerable flexibility with which items in WM can be represented depending upon context. They have important consequences for emerging state-dependent models of WM.

[1]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[2]  H Sompolinsky,et al.  Simple models for reading neuronal population codes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[4]  I. Neath Distinctiveness and serial position effects in recognition , 1993, Memory & cognition.

[5]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[6]  John Jonides,et al.  Trisecting representational states in short-term memory , 2013, Front. Hum. Neurosci..

[7]  Nao Ninomiya,et al.  Visualization is magic! , 2008, J. Vis..

[8]  Paul M. Bays,et al.  Rapid Forgetting Prevented by Retrospective Attention Cues , 2012, Journal of experimental psychology. Human perception and performance.

[9]  A. Nobre,et al.  Orienting Attention to Locations in Internal Representations , 2003, Journal of Cognitive Neuroscience.

[10]  Paul M Bays,et al.  Dynamic Updating of Working Memory Resources for Visual Objects , 2011, The Journal of Neuroscience.

[11]  Paul M Bays,et al.  The precision of visual working memory is set by allocation of a shared resource. , 2009, Journal of vision.

[12]  T. Pasternak,et al.  The multiple roles of visual cortical areas MT/MST in remembering the direction of visual motion. , 2000, Cerebral cortex.

[13]  H. Spekreijse,et al.  Large capacity storage of integrated objects before change blindness , 2003, Vision Research.

[14]  M. Husain,et al.  Attention is Required for Maintenance of Feature Binding in Visual Working Memory , 2014, Quarterly journal of experimental psychology.

[15]  R. Romo,et al.  Neuronal Population Coding of Parametric Working Memory , 2010, The Journal of Neuroscience.

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

[17]  D. Hay,et al.  Serial position effects in short-term visual memory: A SIMPLE explanation? , 2007, Memory & cognition.

[18]  John Jonides,et al.  Neural correlates of access to short-term memory , 2008, Proceedings of the National Academy of Sciences.

[19]  Lisa Durrance Blalock,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Encoding and Representation of Simultaneous and Sequential Arrays in Visuospatial Working Memory , 2022 .

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

[21]  Yuhong Jiang,et al.  Distributing versus focusing attention in visual short-term memory , 2007, Psychonomic bulletin & review.

[22]  Gustavo Deco,et al.  Effective Visual Working Memory Capacity: An Emergent Effect from the Neural Dynamics in an Attractor Network , 2012, PloS one.

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

[24]  Bahador Bahrami,et al.  Precision of working memory for visual motion sequences and transparent motion surfaces. , 2011, Journal of vision.

[25]  Pablo Campo,et al.  Working memory retrieval differences between medial temporal lobe epilepsy patients and controls: A three memory layer approach , 2014, Brain and Cognition.

[26]  Victor A. F. Lamme,et al.  Detailed Sensory Memory, Sloppy Working Memory , 2010, Front. Psychology.

[27]  Klaus Oberauer,et al.  Decoding Attended Information in Short-term Memory: An EEG Study , 2013, Journal of Cognitive Neuroscience.

[28]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[29]  Xiao-Jing Wang,et al.  From Distributed Resources to Limited Slots in Multiple-Item Working Memory: A Spiking Network Model with Normalization , 2012, The Journal of Neuroscience.

[30]  B. McElree,et al.  Attended and Non-Attended States in Working Memory: Accessing Categorized Structures , 1998 .

[31]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[32]  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..

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

[34]  Lila Davachi,et al.  Are Representations in Working Memory Distinct From Representations in Long-Term Memory? , 2010, Psychological science.

[35]  A. Nobre,et al.  Attentional modulation of object representations in working memory. , 2007, Cerebral cortex.

[36]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[37]  Razvan Pascanu,et al.  A neurodynamical model for working memory , 2011, Neural Networks.

[38]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[39]  A. Nobre,et al.  Modulation of working-memory maintenance by directed attention , 2011, Neuropsychologia.

[40]  K. Oberauer,et al.  Focused, unfocused, and defocused information in working memory. , 2013, Journal of experimental psychology. Learning, memory, and cognition.

[41]  N. Cowan Attention and Memory: An Integrated Framework , 1995 .

[42]  Matthew F. S. Rushworth,et al.  Frontal and Parietal Cortical Interactions with Distributed Visual Representations during Selective Attention and Action Selection , 2013, The Journal of Neuroscience.

[43]  Klaus Oberauer,et al.  Neural Evidence for a Distinction between Short-term Memory and the Focus of Attention , 2012, Journal of Cognitive Neuroscience.

[44]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[45]  B. Dosher,et al.  Serial Retrieval Processes in the Recovery of Order Information , 1993 .

[46]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[47]  K. Oberauer Access to information in working memory: exploring the focus of attention. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[48]  John Jonides,et al.  Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory , 2011, NeuroImage.

[49]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[50]  S. Luck,et al.  Attention effects during visual short-term memory maintenance: Protection or prioritization? , 2007 .

[51]  K. Oberauer Binding and inhibition in working memory: individual and age differences in short-term recognition. , 2005, Journal of experimental psychology. General.

[52]  J. Fellous,et al.  A role for NMDA-receptor channels in working memory , 1998, Nature Neuroscience.

[53]  W. Maass,et al.  State-dependent computations: spatiotemporal processing in cortical networks , 2009, Nature Reviews Neuroscience.

[54]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[55]  Masud Husain,et al.  Causal Evidence for a Privileged Working Memory State in Early Visual Cortex , 2014, The Journal of Neuroscience.

[56]  Victor A. F. Lamme,et al.  Are There Multiple Visual Short-Term Memory Stores? , 2008, PloS one.

[57]  Lila Davachi,et al.  Working Memory Retrieval: Contributions of the Left Prefrontal Cortex, the Left Posterior Parietal Cortex, and the Hippocampus , 2009, Journal of Cognitive Neuroscience.

[58]  Lauren L. Richmond,et al.  Shifting Attention among Working Memory Representations: Testing Cue Type, Awareness, and Strategic Control , 2012, Quarterly journal of experimental psychology.

[59]  A. Nobre,et al.  Spatial Selection of Features within Perceived and Remembered Objects , 2009, NeuroImage.

[60]  N. Zokaei Modulation of working memory , 2013 .

[61]  B. Dosher,et al.  Serial position and set size in short-term memory: The time course of recognition , 1989 .

[62]  Klaus Oberauer,et al.  Design for a working memory. , 2009 .