Probing the limits of activity-silent non-conscious working memory

Two types of working memory (WM) have recently been proposed: conscious active WM, depending on sustained neural activity, and activity-silent WM, requiring neither conscious awareness nor accompanying neural activity. However, whether both states support identical forms of information processing is unknown. Theory predicts that activity-silent states are confined to passive storage and cannot operate on stored information. To determine whether an explicit reactivation is required prior to the manipulation of information in WM, we evaluated whether participants could mentally rotate brief visual stimuli of variable subjective visibility. Behaviorally, even for unseen targets, subjects reported the rotated location above chance after several seconds. As predicted, however, such blindsight performance was accompanied by neural signatures of conscious reactivation at the time of mental rotation, including a sustained desynchronization in alpha/beta frequency and a decodable representation of participants’ guess and response. Our findings challenge the concept of genuine non-conscious “working” memory, argue that activity-silent states merely support passive short-term memory, and provide a cautionary note for purely behavioral studies of non-conscious information processing.

[1]  S. Dehaene,et al.  Distinct cortical codes and temporal dynamics for conscious and unconscious percepts , 2015, eLife.

[2]  B. Baars,et al.  How conscious experience and working memory interact , 2003, Trends in Cognitive Sciences.

[3]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

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

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

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

[7]  S. Dehaene,et al.  Time-Resolved Decoding of Two Processing Chains during Dual-Task Interference , 2015, Neuron.

[8]  Shintaro Funahashi,et al.  Prefrontal delay-period activity reflects the decision process of a saccade direction during a free-choice ODR task. , 2007, Cerebral cortex.

[9]  J. Eriksson,et al.  Maintenance of non-consciously presented information engages the prefrontal cortex , 2014, Front. Hum. Neurosci..

[10]  Stanislas Dehaene,et al.  The cognitive architecture for chaining of two mental operations , 2009, Cognition.

[11]  S. Dehaene,et al.  Timing of the brain events underlying access to consciousness during the attentional blink , 2005, Nature Neuroscience.

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

[13]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[14]  P. Roelfsema,et al.  The threshold for conscious report: Signal loss and response bias in visual and frontal cortex , 2018, Science.

[15]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[16]  M. Tsodyks,et al.  A theory of working memory without consciousness or sustained activity , 2016, bioRxiv.

[17]  S. Funahashi,et al.  Stable and Dynamic Coding for Working Memory in Primate Prefrontal Cortex , 2017, The Journal of Neuroscience.

[18]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[19]  Juha Silvanto,et al.  Working Memory Maintenance: Sustained Firing or Synaptic Mechanisms? , 2017, Trends in Cognitive Sciences.

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

[21]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

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

[23]  Juha Silvanto,et al.  Working memory without consciousness , 2011, Current Biology.

[24]  Jonathan W. Pillow,et al.  Single-trial spike trains in parietal cortex reveal discrete steps during decision-making , 2015, Science.

[25]  S. Funahashi,et al.  Neural mechanisms of dual-task interference and cognitive capacity limitation in the prefrontal cortex , 2014, Nature Neuroscience.

[26]  Juha Silvanto,et al.  Metacognition of Visual Short-Term Memory: Dissociation between Objective and Subjective Components of VSTM , 2013, Front. Psychology.

[27]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[28]  S. Dehaene,et al.  Brain Mechanisms Underlying the Brief Maintenance of Seen and Unseen Sensory Information , 2016, Neuron.

[29]  S. Dehaene,et al.  Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework , 2001, Cognition.

[30]  R. Shepard,et al.  Mental Rotation of Three-Dimensional Objects , 1971, Science.

[31]  Florent Meyniel,et al.  Better Get Back to Work: A Role for Motor Beta Desynchronization in Incentive Motivation , 2014, The Journal of Neuroscience.

[32]  J. Eriksson,et al.  Neural Evidence for Non-conscious Working Memory , 2018, Cerebral cortex.

[33]  S. Dehaene,et al.  Unconscious semantic priming extends to novel unseen stimuli , 2001, Cognition.

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

[35]  S. Dehaene,et al.  Temporal-order information can be maintained in non-conscious working memory , 2019, Scientific Reports.

[36]  Claude Alain,et al.  Neural Dynamics Underlying Attentional Orienting to Auditory Representations in Short-Term Memory , 2015, The Journal of Neuroscience.

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

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

[39]  N. Kanwisher,et al.  Attention as inference: selection is probabilistic; responses are all-or-none samples. , 2009, Journal of experimental psychology. General.

[40]  M. Overgaard,et al.  Introspection and subliminal perception , 2004 .

[41]  E. Miller,et al.  Gamma and Beta Bursts Underlie Working Memory , 2016, Neuron.

[42]  E. Vogel,et al.  Visual working memory capacity: from psychophysics and neurobiology to individual differences , 2013, Trends in Cognitive Sciences.

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

[44]  A. Mamelak,et al.  Persistently active neurons in human medial frontal and medial temporal lobe support working memory , 2017, Nature Neuroscience.

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

[46]  Eelke Spaak,et al.  The Importance of Single-Trial Analyses in Cognitive Neuroscience , 2016, Trends in Cognitive Sciences.

[47]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[48]  Nicolas Y. Masse,et al.  Circuit mechanisms for the maintenance and manipulation of information in working memory , 2018 .

[49]  Stanislas Dehaene,et al.  Neural capacity limits during unconscious semantic processing , 2018, The European journal of neuroscience.

[50]  Dominique Lamy,et al.  Neural Correlates of Subjective Awareness and Unconscious Processing: An ERP Study , 2009, Journal of Cognitive Neuroscience.

[51]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

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

[53]  L. Cooper Mental rotation of random two-dimensional shapes , 1975, Cognitive Psychology.

[54]  Albert Costa,et al.  Set size and repetition in the picture–word interference paradigm: implications for models of naming , 2001, Cognition.

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

[56]  H. Heinze,et al.  Cortical Activations during the Mental Rotation of Different Visual Objects , 2001, NeuroImage.

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

[58]  Romain Quentin,et al.  Differential Brain Mechanisms of Selection and Maintenance of Information during Working Memory , 2018, The Journal of Neuroscience.

[59]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[60]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[61]  Isabel Gauthier,et al.  BOLD Activity during Mental Rotation and Viewpoint-Dependent Object Recognition , 2002, Neuron.

[62]  Johan Eriksson,et al.  The conjunction of non-consciously perceived object identity and spatial position can be retained during a visual short-term memory task , 2015, Front. Psychol..

[63]  Simon van Gaal,et al.  Unconscious Activation of the Prefrontal No-Go Network , 2010, The Journal of Neuroscience.