Occipital sleep spindles predict sequence learning in a visuo-motor task

Abstract Study Objectives The brain appears to use internal models to successfully interact with its environment via active predictions of future events. Both internal models and the predictions derived from them are based on previous experience. However, it remains unclear how previously encoded information is maintained to support this function, especially in the visual domain. In the present study, we hypothesized that sleep consolidates newly encoded spatio-temporal regularities to improve predictions afterwards. Methods We tested this hypothesis using a novel sequence-learning paradigm that aimed to dissociate perceptual from motor learning. We recorded behavioral performance and high-density electroencephalography (EEG) in male human participants during initial training and during testing two days later, following an experimental night of sleep (n = 16, including high-density EEG recordings) or wakefulness (n = 17). Results Our results show sleep-dependent behavioral improvements correlated with sleep-spindle activity specifically over occipital cortices. Moreover, event-related potential (ERP) responses indicate a shift of attention away from predictable to unpredictable sequences after sleep, consistent with enhanced automaticity in the processing of predictable sequences. Conclusions These findings suggest a sleep-dependent improvement in the prediction of visual sequences, likely related to visual cortex reactivation during sleep spindles. Considering that controls in our experiments did not fully exclude oculomotor contributions, future studies will need to address the extent to which these effects depend on purely perceptual versus oculomotor sequence learning.

[1]  R. Spencer,et al.  Memory and the circadian system: Identifying candidate mechanisms by which local clocks in the brain may regulate synaptic plasticity , 2020, Neuroscience & Biobehavioral Reviews.

[2]  K. Rauss,et al.  Anatomic and functional asymmetries interactively shape human early visual cortex responses , 2020, Journal of vision.

[3]  T. Dang-Vu,et al.  Brain Rhythms During Sleep and Memory Consolidation: Neurobiological Insights. , 2020, Physiology.

[4]  Itamar Lerner,et al.  Sleep and the extraction of hidden regularities: A systematic review and the importance of temporal rules. , 2019, Sleep medicine reviews.

[5]  Jens G. Klinzing,et al.  Mechanisms of systems memory consolidation during sleep , 2019, Nature Neuroscience.

[6]  N. Censor,et al.  Visual-oculomotor interactions facilitate consolidation of perceptual learning. , 2019, Journal of vision.

[7]  A. Ballesio,et al.  Updating Internal Cognitive Models during Sleep , 2019, The Journal of Neuroscience.

[8]  Bernhard P. Staresina,et al.  Sleep Spindles and Memory Reprocessing , 2019, Trends in Neurosciences.

[9]  P. Enticott,et al.  Visuospatial sequence learning on the serial reaction time task modulates the P1 event-related potential. , 2018, Psychophysiology.

[10]  J. Born,et al.  Cortical circuit activity underlying sleep slow oscillations and spindles , 2018, Proceedings of the National Academy of Sciences.

[11]  Jan Born,et al.  Sleep Strengthens Predictive Sequence Coding , 2018, The Journal of Neuroscience.

[12]  Jochen Triesch,et al.  Bridging structure and function: A model of sequence learning and prediction in primary visual cortex , 2018, PLoS Comput. Biol..

[13]  Karolina Janacsek,et al.  ERPs differentiate the sensitivity to statistical probabilities and the learning of sequential structures during procedural learning , 2018, Biological Psychology.

[14]  I. Wilhelm,et al.  Children's initial sleep-associated changes in motor skill are unrelated to long-term skill levels. , 2017, Developmental science.

[15]  Aneesha K. Suresh,et al.  Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity , 2017, Proceedings of the National Academy of Sciences.

[16]  R. Verleger,et al.  Sleep Spindles in the Right Hemisphere Support Awareness of Regularities and Reflect Pre-Sleep Activations , 2017, Sleep.

[17]  Serge O. Dumoulin,et al.  Radial asymmetries in population receptive field size and cortical magnification factor in early visual cortex , 2018, NeuroImage.

[18]  Genevieve Albouy,et al.  Sleeping on the motor engram: The multifaceted nature of sleep-related motor memory consolidation , 2017, Neuroscience & Biobehavioral Reviews.

[19]  Carryl L. Baldwin,et al.  Detecting and Quantifying Mind Wandering during Simulated Driving , 2017, Front. Hum. Neurosci..

[20]  M. Frank Sleep and plasticity in the visual cortex: more than meets the eye , 2017, Current Opinion in Neurobiology.

[21]  Edwin M. Robertson,et al.  Dual enhancement mechanisms for overnight motor memory consolidation , 2017, Nature Human Behaviour.

[22]  Karl J. Friston,et al.  Is predictability salient? A study of attentional capture by auditory patterns , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Chih-Yang Chen,et al.  Sharper, Stronger, Faster Upper Visual Field Representation in Primate Superior Colliculus , 2016, Current Biology.

[24]  Oxana Eschenko,et al.  Ripple-triggered stimulation of the locus coeruleus during post-learning sleep disrupts ripple/spindle coupling and impairs memory consolidation , 2016, Learning & memory.

[25]  Penelope A. Lewis,et al.  Cross-modal transfer of statistical information benefits from sleep , 2016, Cortex.

[26]  P. Lewis,et al.  Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity , 2016, PLoS biology.

[27]  J. Born,et al.  Increasing Explicit Sequence Knowledge by Odor Cueing during Sleep in Men but not Women , 2016, Front. Behav. Neurosci..

[28]  D. Ulrich Sleep Spindles as Facilitators of Memory Formation and Learning , 2016, Neural plasticity.

[29]  Christopher Kennard,et al.  Learning and Recognition of a Non-conscious Sequence of Events in Human Primary Visual Cortex , 2016, Current Biology.

[30]  Michael M. Halassa,et al.  Thalamic Circuit Mechanisms Link Sensory Processing in Sleep and Attention , 2016, Front. Neural Circuits.

[31]  R. Verleger,et al.  Is insight a godsend? Explicit knowledge in the serial response-time task has precursors in EEG potentials already at task onset , 2015, Neurobiology of Learning and Memory.

[32]  K. Ganguly,et al.  Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation , 2015, PLoS biology.

[33]  P. Lewis,et al.  Cued Memory Reactivation during Slow-Wave Sleep Promotes Explicit Knowledge of a Motor Sequence , 2014, The Journal of Neuroscience.

[34]  Lucia M. Talamini,et al.  Local sleep spindle modulations in relation to specific memory cues , 2014, NeuroImage.

[35]  G. Stefanics,et al.  Visual mismatch negativity: a predictive coding view , 2014, Front. Hum. Neurosci..

[36]  Mark R Schultz,et al.  False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. , 2014, Journal of clinical epidemiology.

[37]  Takeo Watanabe,et al.  Location specific sleep spindle activity in the early visual areas and perceptual learning , 2014, Vision Research.

[38]  Sunbin Song,et al.  Practice and sleep form different aspects of skill , 2014, Nature Communications.

[39]  N. Fogelson,et al.  Local contextual processing in major depressive disorder , 2014, Clinical Neurophysiology.

[40]  Lisa Genzel,et al.  Diminished Nap Effects on Memory Consolidation Are Seen Under Oral Contraceptive Use , 2014, Neuropsychobiology.

[41]  R. Spencer,et al.  Age-related changes in consolidation of perceptual and muscle-based learning of motor skills , 2013, Front. Aging Neurosci..

[42]  P. Lewis,et al.  Overnight consolidation aids the transfer of statistical knowledge from the medial temporal lobe to the striatum. , 2013, Cerebral cortex.

[43]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[44]  G. Pourtois,et al.  What is Bottom-Up and What is Top-Down in Predictive Coding? , 2013, Front. Psychol..

[45]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[46]  Karolina Janacsek,et al.  The differential consolidation of perceptual and motor learning in skill acquisition , 2013, Cortex.

[47]  Elizabeth A. McDevitt,et al.  The Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study , 2013, The Journal of Neuroscience.

[48]  Xiaorong Gao,et al.  Learning without consciously knowing: Evidence from event-related potentials in sequence learning , 2013, Consciousness and Cognition.

[49]  G. Albouy,et al.  Daytime Sleep Enhances Consolidation of the Spatial but Not Motoric Representation of Motor Sequence Memory , 2013, PloS one.

[50]  J. Born,et al.  Skill Memory Escaping from Distraction by Sleep—Evidence from Dual-Task Performance , 2012, PloS one.

[51]  Nicholas B Turk-Browne,et al.  Statistical learning and its consequences. , 2012, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[52]  L. Brown Can sleep deprivation studies explain why human adults sleep? , 2012, Current opinion in pulmonary medicine.

[53]  Nick F Ramsey,et al.  Sleep spindles are locally modulated by training on a brain–computer interface , 2012, Proceedings of the National Academy of Sciences.

[54]  I. Timofeev,et al.  Sleep Oscillations in the Thalamocortical System Induce Long-Term Neuronal Plasticity , 2012, Neuron.

[55]  Janneke F. M. Jehee,et al.  Attention Reverses the Effect of Prediction in Silencing Sensory Signals , 2011, Cerebral cortex.

[56]  Karl J. Friston,et al.  Predictive coding, precision and synchrony , 2012, Cognitive neuroscience.

[57]  M. Dresler,et al.  Sex and modulatory menstrual cycle effects on sleep related memory consolidation , 2012, Psychoneuroendocrinology.

[58]  Hillary D. Schwarb,et al.  Generalized lessons about sequence learning from the study of the serial reaction time task , 2012, Advances in cognitive psychology.

[59]  Hartwig R. Siebner,et al.  Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations , 2012, NeuroImage.

[60]  J. Born,et al.  Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. , 2011, Sleep.

[61]  J. Born,et al.  Sleep after Vaccination Boosts Immunological Memory , 2011, The Journal of Immunology.

[62]  I. Wilhelm,et al.  System consolidation of memory during sleep , 2011, Psychological research.

[63]  G. Pourtois,et al.  Top-down effects on early visual processing in humans: A predictive coding framework , 2011, Neuroscience & Biobehavioral Reviews.

[64]  Penelope A. Lewis,et al.  Sleep-dependent consolidation of statistical learning , 2011, Neuropsychologia.

[65]  Penelope A. Lewis,et al.  Keeping time in your sleep: Overnight consolidation of temporal rhythm , 2011, Neuropsychologia.

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

[67]  H. Kojima,et al.  The what and why of perceptual asymmetries in the visual domain , 2010, Advances in cognitive psychology.

[68]  J. Gerstner,et al.  Circadian rhythms and memory formation , 2010, Nature Reviews Neuroscience.

[69]  Miguel Castelo-Branco,et al.  Asymmetry of visual sensory mechanisms: electrophysiological, structural, and psychophysical evidences. , 2010, Journal of vision.

[70]  Stoyan Dimitrov,et al.  Effects of sleep and circadian rhythm on the human immune system , 2010, Annals of the New York Academy of Sciences.

[71]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[72]  C. C. Duncan,et al.  Event-related potentials in clinical research: Guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400 , 2009, Clinical Neurophysiology.

[73]  C. Summerfield,et al.  Expectation (and attention) in visual cognition , 2009, Trends in Cognitive Sciences.

[74]  S. Nagata,et al.  Recovery of Cognitive Performance and Fatigue after One Night of Sleep Deprivation , 2009, Journal of occupational health.

[75]  Takeo Watanabe,et al.  Location-Specific Cortical Activation Changes during Sleep after Training for Perceptual Learning , 2009, Current Biology.

[76]  Jiunn-Horng Kang,et al.  Effects of an irregular bedtime schedule on sleep quality, daytime sleepiness, and fatigue among university students in Taiwan , 2009, BMC public health.

[77]  Andrew Tucker,et al.  The effect of blinks and saccadic eye movements on visual reaction times , 2009, Attention, perception & psychophysics.

[78]  G. Pourtois,et al.  Attentional load modifies early activity in human primary visual cortex , 2009, Human brain mapping.

[79]  M. Tamaki,et al.  Activation of fast sleep spindles at the premotor cortex and parietal areas contributes to motor learning: A study using sLORETA , 2009, Clinical Neurophysiology.

[80]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

[81]  Axel Mecklinger,et al.  Error and Deviance Processing in Implicit and Explicit Sequence Learning , 2008, Journal of Cognitive Neuroscience.

[82]  Yuka Sasaki,et al.  Different Dynamics of Performance and Brain Activation in the Time Course of Perceptual Learning , 2008, Neuron.

[83]  B. Scholl,et al.  Multidimensional Visual Statistical Learning Visual Statistical Learning , 2005 .

[84]  J. Ashe,et al.  Time of day accounts for overnight improvement in sequence learning. , 2007, Learning & memory.

[85]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[86]  E. Robertson The Serial Reaction Time Task: Implicit Motor Skill Learning? , 2007, The Journal of Neuroscience.

[87]  Jonathan R. Folstein,et al.  Influence of cognitive control and mismatch on the N2 component of the ERP: a review. , 2007, Psychophysiology.

[88]  Michael W. Levine,et al.  Magnocellular and parvocellular visual pathway contributions to visual field anisotropies , 2007, Vision Research.

[89]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[90]  Richard B Ivry,et al.  Age-related decline of sleep-dependent consolidation. , 2007, Learning & memory.

[91]  M. Walker,et al.  Daytime Naps, Motor Memory Consolidation and Regionally Specific Sleep Spindles , 2007, PloS one.

[92]  J. Born,et al.  Number and function of circulating human antigen presenting cells regulated by sleep. , 2007, Sleep.

[93]  C. Cajochen,et al.  Circadian rhythms in cognitive performance: Methodological constraints, protocols, theoretical underpinnings , 2007, Physiology & Behavior.

[94]  Stefan Fischer,et al.  Developmental Differences in Sleep's Role for Implicit Off-line Learning: Comparing Children with Adults , 2007, Journal of Cognitive Neuroscience.

[95]  Michael Bach,et al.  The Freiburg Visual Acuity Test-Variability unchanged by post-hoc re-analysis , 2007, Graefe's Archive for Clinical and Experimental Ophthalmology.

[96]  D. Fabó,et al.  Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles , 2006, Neuroscience Letters.

[97]  Christophe Phillips,et al.  Implicit Oculomotor Sequence Learning in Humans: Time Course of Offline Processing , 2022 .

[98]  Richard B. Ivry,et al.  Sleep-Dependent Consolidation of Contextual Learning , 2006, Current Biology.

[99]  D. J. Marcus,et al.  Oculomotor evidence of sequence learning on the serial reaction time task , 2006, Memory & cognition.

[100]  Jan Born,et al.  Implicit Learning–Explicit Knowing: A Role for Sleep in Memory System Interaction , 2006, Journal of Cognitive Neuroscience.

[101]  J. Born,et al.  Sleep-like concentrations of growth hormone and cortisol modulate type1 and type2 in-vitro cytokine production in human T cells. , 2006, International immunopharmacology.

[102]  Alvaro Pascual-Leone,et al.  Off-line learning of motor skill memory: a double dissociation of goal and movement. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[103]  Robert Stickgold,et al.  Cerebral Cortex doi:10.1093/cercor/bhi043 The Functional Anatomy of Sleep-dependent Visual Skill Learning , 2005 .

[104]  L. Peichl Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[105]  Anna C. Nobre,et al.  Synergistic Effect of Combined Temporal and Spatial Expectations on Visual Attention , 2005, The Journal of Neuroscience.

[106]  Á. Pascual-Leone,et al.  Off-Line Learning and the Primary Motor Cortex , 2005, The Journal of Neuroscience.

[107]  Ching-Yu Cheng,et al.  Association of ocular dominance and anisometropic myopia. , 2004, Investigative ophthalmology & visual science.

[108]  Á. Pascual-Leone,et al.  Awareness Modifies the Skill-Learning Benefits of Sleep , 2004, Current Biology.

[109]  J. Born,et al.  Sleep inspires insight , 2004, Nature.

[110]  Steven Laureys,et al.  Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep , 2003, NeuroImage.

[111]  P. Maquet,et al.  Neural correlates of perceptual learning: A functional MRI study of visual texture discrimination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[112]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[113]  R. Knight,et al.  Mechanisms of human attention: event-related potentials and oscillations , 2001, Neuroscience & Biobehavioral Reviews.

[114]  Á. Pascual-Leone,et al.  The role of the dorsolateral prefrontal cortex during sequence learning is specific for spatial information. , 2001, Cerebral cortex.

[115]  R Verleger,et al.  ERP correlates of associative learning. , 2001, Psychophysiology.

[116]  Frank Rösler,et al.  Response Anticipation Processes in the Learning of a Sensorimotor Sequence: Evidence from the Latera , 2001 .

[117]  Á. Pascual-Leone,et al.  Aspects of sensory guidance in sequence learning , 2001, Experimental Brain Research.

[118]  H Barlow,et al.  Redundancy reduction revisited , 2001, Network.

[119]  G. Woodman,et al.  Event-related potential studies of attention , 2000, Trends in Cognitive Sciences.

[120]  Martin Eimer,et al.  Chunking processes in the learning of event sequences: Electrophysiological indicators , 2000, Memory & cognition.

[121]  Axel Cleeremans,et al.  Experience-dependent changes in cerebral activation during human REM sleep , 2000, Nature Neuroscience.

[122]  F Rösler,et al.  Implicit and explicit learning of event sequences: evidence for distinct coding of perceptual and motor representations. , 2000, Acta psychologica.

[123]  Marisa Carrasco,et al.  Attention improves or impairs visual performance by enhancing spatial resolution , 1998, Nature.

[124]  S. Hillyard,et al.  Event-related brain potentials in the study of visual selective attention. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[125]  M Eimer,et al.  Explicit and implicit learning of event sequences: evidence from event-related brain potentials. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[126]  F. Previc Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

[127]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[128]  E. Niedermeyer,et al.  Sleep Spindles , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[129]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[130]  R. Gregory Perceptions as hypotheses. , 1980, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[131]  J. H. Steiger Tests for comparing elements of a correlation matrix. , 1980 .

[132]  W. Dement,et al.  Quantification of sleepiness: a new approach. , 1973, Psychophysiology.

[133]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[134]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[135]  Jan Born,et al.  A Role of Sleep in Forming Predictive Codes , 2017 .

[136]  Si Wu,et al.  Asymmetric representations of upper and lower visual fields in egocentric and allocentric references. , 2017, Journal of vision.

[137]  B. Rasch,et al.  Cognitive Neuroscience of Memory Consolidation , 2017 .

[138]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

[139]  I. Wilhelm,et al.  Sleep to implement an intention. , 2013, Sleep.

[140]  M. Carrasco,et al.  Isoeccentric locations are not equivalent: The extent of the vertical meridian asymmetry , 2012, Vision Research.

[141]  William D S Killgore,et al.  Effects of sleep deprivation on cognition. , 2010, Progress in brain research.

[142]  G. Pourtois,et al.  Effects of perceptual learning on primary visual cortex activity in humans , 2008, Vision Research.

[143]  Rajesh P. N. Rao,et al.  Neurobiology of Attention , 2005 .

[144]  Thomas F Münte,et al.  Differences in incidental and intentional learning of sensorimotor sequences as revealed by event-related brain potentials. , 2003, Brain research. Cognitive brain research.

[145]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[146]  M. Kutas,et al.  An ERP analysis of implicit structured sequence learning. , 1997, Psychophysiology.

[147]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[148]  W. Skrandies The Upper and Lower Visual Field of Man: Electrophysiological and Functional Differences , 1987 .

[149]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[150]  Philip M. Corsi Human memory and the medial temporal region of the brain. , 1972 .