Current and future goals are represented in opposite patterns in object-selective cortex

Adaptive behavior requires the separation of current from future goals in working memory. We used fMRI of object-selective cortex to determine the representational (dis)similarities of memory representations serving current and prospective perceptual tasks. Participants remembered an object drawn from three possible categories as the target for one of two consecutive visual search tasks. A cue indicated whether the target object should be looked for first (currently relevant), second (prospectively relevant), or if it could be forgotten (irrelevant). Prior to the first search, representations of current, prospective and irrelevant objects were similar, with strongest decoding for current representations compared to prospective (Experiment 1) and irrelevant (Experiment 2). Remarkably, during the first search, prospective representations could also be decoded, but revealed anti-correlated voxel patterns compared to currently relevant representations of the same category. We propose that the brain separates current from prospective memories within the same neuronal ensembles through opposite representational patterns.

[1]  Christian N. L. Olivers,et al.  From ERPs to MVPA Using the Amsterdam Decoding and Modeling Toolbox (ADAM) , 2018, Front. Neurosci..

[2]  Alexander G. Huth,et al.  Attention During Natural Vision Warps Semantic Representation Across the Human Brain , 2013, Nature Neuroscience.

[3]  Elkan G. Akyürek,et al.  Dynamic hidden states underlying working memory guided behaviour , 2017, Nature Neuroscience.

[4]  Adam C. Riggall,et al.  Reactivation of latent working memories with transcranial magnetic stimulation , 2016, Science.

[5]  Zheng Liu,et al.  Short-Term Memory Trace in Rapidly Adapting Synapses of Inferior Temporal Cortex , 2008, PLoS Comput. Biol..

[6]  Joram van Driel,et al.  Priority Switches in Visual Working Memory are Supported by Frontal Delta and Posterior Alpha Interactions , 2018, Cerebral cortex.

[7]  Jonas Larsson,et al.  fMRI repetition suppression: neuronal adaptation or stimulus expectation? , 2012, Cerebral cortex.

[8]  Jarrod A. Lewis-Peacock,et al.  Decoding the internal focus of attention , 2012, Neuropsychologia.

[9]  M. Chun,et al.  Linking Implicit and Explicit Memory: Common Encoding Factors and Shared Representations , 2006, Neuron.

[10]  M. Stokes.  ‘Activity-silent’ working memory in prefrontal cortex: a dynamic coding framework , 2015, Trends in Cognitive Sciences.

[11]  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.

[12]  R. VanRullen,et al.  Attention and biased competition in multi-voxel object representations , 2009, Proceedings of the National Academy of Sciences.

[13]  Marie T. Banich,et al.  Multiple modes of clearing one's mind of current thoughts: Overlapping and distinct neural systems , 2015, Neuropsychologia.

[14]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[15]  Nancy B. Carlisle,et al.  Automatic and strategic effects in the guidance of attention by working memory representations. , 2011, Acta psychologica.

[16]  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..

[17]  Dwight J. Kravitz,et al.  Goal-dependent dissociation of visual and prefrontal cortices during working memory , 2013, Nature Neuroscience.

[18]  Brice A. Kuhl,et al.  Repetition Suppression and Multi-Voxel Pattern Similarity Differentially Track Implicit and Explicit Visual Memory , 2013, The Journal of Neuroscience.

[19]  B. Postle,et al.  The cognitive neuroscience of working memory. , 2007, Annual review of psychology.

[20]  C. Allefeld,et al.  Cortical specialization for attended versus unattended working memory , 2018, Nature Neuroscience.

[21]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

[22]  B. Postle,et al.  Different states of priority recruit different neural codes in visual working memory , 2018, bioRxiv.

[23]  G. McCarthy,et al.  Evidence for a Refractory Period in the Hemodynamic Response to Visual Stimuli as Measured by MRI , 2000, NeuroImage.

[24]  A. Nobre,et al.  Prioritizing Information during Working Memory: Beyond Sustained Internal Attention , 2017, Trends in Cognitive Sciences.

[25]  P. Roelfsema,et al.  The effect of items in working memory on the deployment of attention and the eyes during visual search. , 2006, Journal of experimental psychology. Human perception and performance.

[26]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

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

[28]  I. Toni,et al.  Shared Representations for Working Memory and Mental Imagery in Early Visual Cortex , 2013, Current Biology.

[29]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[30]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

[32]  Nicholas E. Myers,et al.  Revealing hidden states in visual working memory using electroencephalography , 2015, Front. Syst. Neurosci..

[33]  S. Dehaene,et al.  Characterizing the dynamics of mental representations: the temporal generalization method , 2014, Trends in Cognitive Sciences.

[34]  Nicole C. Rust,et al.  Single-exposure visual memory judgments are reflected in inferotemporal cortex , 2018, eLife.

[35]  Samuel A. Nastase,et al.  Attention Selectively Reshapes the Geometry of Distributed Semantic Representation , 2016, bioRxiv.

[36]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[37]  Stefan Pollmann,et al.  Cortical evidence for negative search templates , 2017 .

[38]  Christian N L Olivers,et al.  Subtle eye movement metrics reveal task-relevant representations prior to visual search. , 2017, Journal of vision.

[39]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[40]  Paul E. Downing,et al.  Competition in visual working memory for control of search , 2003 .

[41]  M. Tsodyks,et al.  Working models of working memory , 2014, Current Opinion in Neurobiology.

[42]  Adam C. Riggall,et al.  Within-Category Decoding of Information in Different Attentional States in Short-Term Memory , 2016, Cerebral cortex.

[43]  John Lisman,et al.  A Single Brief Burst Induces GluR1-dependent Associative Short-term Potentiation: A Potential Mechanism for Short-term Memory , 2010, Journal of Cognitive Neuroscience.

[44]  Sebastian Schneegans,et al.  Restoration of fMRI Decodability Does Not Imply Latent Working Memory States , 2017, Journal of Cognitive Neuroscience.

[45]  R. Vautin,et al.  Responses of single cells in cat visual cortex to prolonged stimulus movement: neural correlates of visual aftereffects. , 1977, Journal of neurophysiology.

[46]  R. Goebel,et al.  Task-Relevant and Accessory Items in Working Memory Have Opposite Effects on Activity in Extrastriate Cortex , 2012, The Journal of Neuroscience.

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

[48]  M. Eimer,et al.  On the difference between working memory and attentional set , 2011, Neuropsychologia.

[49]  Edward F. Ester,et al.  Restoring Latent Visual Working Memory Representations in Human Cortex , 2016, Neuron.

[50]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[51]  P. Roelfsema,et al.  Different States in Visual Working Memory: When It Guides Attention and When It Does Not , 2022 .

[52]  Dwight J. Kravitz,et al.  Task context impacts visual object processing differentially across the cortex , 2014, Proceedings of the National Academy of Sciences.

[53]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[54]  T. Curran,et al.  Prefrontal Regions Orchestrate Suppression of Emotional Memories via a Two-Phase Process , 2007, Science.

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

[56]  Michael C. Anderson,et al.  Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression , 2015, Nature Neuroscience.

[57]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.