Predicting the future: from implicit learning to consolidation.

Sequence learning can be differentiated according to phases (rapid and slower), modalities (perceptual and motor), and whether or not it is conscious (implicit and explicit). Implicit sequence learning occurs when information is acquired from an environment of complex stimuli without conscious access either to what was learned or to the fact that learning occurred. In everyday life, this learning mechanism is crucial for adapting to the environment and for predicting events unconsciously. Implicit sequence learning underlies not only motor, but also cognitive and social skills; it is therefore an important aspect of life from infancy to old age. Moreover, this kind of learning does not occur only during practice, in the so-called online periods, but also between practice periods, during the so-called offline periods. The process that occurs during the offline periods is referred to as consolidation, which denotes the stabilization of a memory trace after the initial acquisition; this can result in increased resistance to interference or even improvement in performance following an offline period. Understanding the multiple aspects and influencing factors of consolidation can help us to reveal the nature of memory and changes in brain plasticity. Our review focuses on how consolidation varies with factors such as awareness, the length of offline periods, the type of information to be learned, and the age of participants. We highlight that consolidation is not a single process; instead, there are multiple mechanisms in the offline period, which are differently influenced by these factors.

[1]  M. Ziessler,et al.  Learning of event sequences is based on response-effect learning: further evidence from a serial reaction task. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[2]  Daniel Z. Press,et al.  Sequence Skill Acquisition and Off-Line Learning in Normal Aging , 2009, PloS one.

[3]  Heidi Johansen-Berg,et al.  Model-free characterization of brain functional networks for motor sequence learning using fMRI , 2008, NeuroImage.

[4]  A. Karni,et al.  Dependence on REM sleep of overnight improvement of a perceptual skill. , 1994, Science.

[5]  R. Stickgold,et al.  Sleep and memory: the ongoing debate. , 2005, Sleep.

[6]  R. Poldrack,et al.  How do memory systems interact? Evidence from human classification learning , 2004, Neurobiology of Learning and Memory.

[7]  M. Desseilles,et al.  Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory , 2008, Neuron.

[8]  J. Krakauer,et al.  Consolidation of motor memory , 2006, Trends in Neurosciences.

[9]  Axel Cleeremans,et al.  Implicit learning: news from the front , 1998, Trends in Cognitive Sciences.

[10]  Ferenc Kemény,et al.  Perceptual Effect on Motor Learning in the Serial Reaction-Time Task , 2011, The Journal of general psychology.

[11]  P. Bosco,et al.  The APOE e4 allele increases the risk of impaired spatial working memory in obstructive sleep apnea , 2008 .

[12]  Leslie G. Ungerleider,et al.  Brain plasticity related to the consolidation of motor sequence learning and motor adaptation , 2010, Proceedings of the National Academy of Sciences.

[13]  E. Heerey,et al.  Implicit learning of social predictions , 2010 .

[14]  M. Gluck,et al.  How do people solve the "weather prediction" task?: individual variability in strategies for probabilistic category learning. , 2002, Learning & memory.

[15]  S. Keele,et al.  The cognitive and neural architecture of sequence representation. , 2003, Psychological review.

[16]  J. Doyon Motor sequence learning and movement disorders , 2008, Current opinion in neurology.

[17]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[18]  J. Hobson,et al.  The prefrontal cortex in sleep , 2002, Trends in Cognitive Sciences.

[19]  Guinevere F. Eden,et al.  Dyslexics are impaired on implicit higher-order sequence learning, but not on implicit spatial context learning , 2006, Neuropsychologia.

[20]  J. H. Howard,et al.  Age differences in implicit learning of higher order dependencies in serial patterns. , 1997, Psychology and aging.

[21]  J. Pépin,et al.  Which memory processes are affected in patients with obstructive sleep apnea? An evaluation of 3 types of memory. , 2006, Sleep.

[22]  R. Stickgold,et al.  Linking brain and behavior in sleep-dependent learning and memory consolidation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  D. Shanks IMPLICIT LEARNING AND TACIT KNOWLEDGE - AN ESSAY ON THE COGNITIVE UNCONSCIOUS - REBER,A , 1995 .

[25]  J. H. Howard,et al.  Adult age differences in the rate of learning serial patterns: evidence from direct and indirect tests. , 1992, Psychology and aging.

[26]  Sunbin Song,et al.  Sleep Does Not Benefit Probabilistic Motor Sequence Learning , 2007, The Journal of Neuroscience.

[27]  Peter A. Frensch,et al.  One concept, multiple meanings: On how to define the concept of implicit learning. , 1998 .

[28]  M. Chun,et al.  Contextual Cueing: Implicit Learning and Memory of Visual Context Guides Spatial Attention , 1998, Cognitive Psychology.

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

[30]  Z. Mari,et al.  Intact implicit probabilistic sequence learning in obstructive sleep apnea , 2012, Journal of sleep research.

[31]  Daniel B. Willingham,et al.  Implicit motor sequence learning is not purely perceptual , 1999, Memory & cognition.

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

[33]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

[34]  Lars Bäckman,et al.  Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: Relations to performance , 2010, NeuroImage.

[35]  J. García-Moncó,et al.  Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions , 2008, Clinical Neurology and Neurosurgery.

[36]  Matthew D. Lieberman,et al.  Intuition: a social cognitive neuroscience approach. , 2000, Psychological bulletin.

[37]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[38]  F. Richer,et al.  Obstructive sleep apnea syndrome: pathogenesis of neuropsychological deficits. , 1991, Journal of clinical and experimental neuropsychology.

[39]  Jennifer C. Romano,et al.  One-year retention of general and sequence-specific skills in a probabilistic, serial reaction time task , 2010, Memory.

[40]  Julia Uddén,et al.  The Neuropharmacology of Implicit Learning , 2010, Current neuropharmacology.

[41]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[42]  Edwin M Robertson,et al.  Off-Line Processing: Reciprocal Interactions between Declarative and Procedural Memories , 2007, The Journal of Neuroscience.

[43]  N. Gosselin,et al.  Attentional deficits in patients with obstructive sleep apnea syndrome: An event-related potential study , 2006, Clinical Neurophysiology.

[44]  Tim Curran,et al.  Effects of aging on implicit sequence learning: Accounting for sequence structure and explicit knowledge , 1997, Psychological research.

[45]  F. Richer,et al.  Persistent neuropsychological deficits and vigilance impairment in sleep apnea syndrome after treatment with continuous positive airways pressure (CPAP). , 1993, Journal of clinical and experimental neuropsychology.

[46]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[47]  Tamar Flash,et al.  Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Zsuzsa Londe,et al.  Learning in Autism: Implicitly Superb , 2010, PloS one.

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

[50]  Lars Bäckman,et al.  Implicit Learning in Aging: Extant Patterns and New Directions , 2009, Neuropsychology Review.

[51]  Zsuzsa Londe,et al.  Perceptual and motor factors of implicit skill learning , 2009, Neuroreport.

[52]  Beat Meier,et al.  What matters in implicit task sequence learning: perceptual stimulus features, task sets, or correlated streams of information? , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[53]  J. Hobson,et al.  REM sleep and dreaming: towards a theory of protoconsciousness , 2009, Nature Reviews Neuroscience.

[54]  Ildikó Hoffmann,et al.  The role of the putamen in cognitive functions — A case study , 2009 .

[55]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[56]  K. Henke A model for memory systems based on processing modes rather than consciousness , 2010, Nature Reviews Neuroscience.

[57]  N J Douglas,et al.  Cognitive function in the sleep apnea/hypopnea syndrome (SAHS). , 2000, Sleep.

[58]  M. Ullman Contributions of memory circuits to language: the declarative/procedural model , 2004, Cognition.

[59]  R. Stickgold,et al.  Sleep and the time course of motor skill learning. , 2003, Learning & memory.

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

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

[62]  F. Fanfulla,et al.  A multidimensional assessment of obese patients with obstructive sleep apnoea syndrome (OSAS): a study of psychological, neuropsychological and clinical relationships in a disabling multifaceted disease. , 2008, Sleep medicine.

[63]  Karolina Janacsek,et al.  Sleep has no critical role in implicit motor sequence learning in young and old adults , 2010, Experimental Brain Research.

[64]  U. Mayr,et al.  Spatial attention and implicit sequence learning: evidence for independent learning of spatial and nonspatial sequences. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[65]  Karen Z. H. Li,et al.  A comparison of motor skill learning and retention in younger and older adults , 2009, Experimental Brain Research.

[66]  B. Meier,et al.  Are correlated streams of information necessary for implicit sequence learning? , 2010, Acta psychologica.

[67]  A. Schulz,et al.  Oral cortisol impairs implicit sequence learning , 2011, Psychopharmacology.

[68]  Alvaro Pascual-Leone,et al.  The time course of off-line motor sequence learning. , 2005, Brain research. Cognitive brain research.

[69]  A. Karni,et al.  Daytime sleep condenses the time course of motor memory consolidation , 2007, Nature Neuroscience.

[70]  J. Born,et al.  Motor Memory Consolidation in Sleep Shapes More Effective Neuronal Representations , 2005, The Journal of Neuroscience.

[71]  Á. Lukács,et al.  The effects of feature analysis, transparency in probabilistic category learning in adults and children , 2009 .

[72]  L. Boyd,et al.  Does Sleep Promote Motor Learning? Implications for Physical Rehabilitation , 2009, Physical Therapy.

[73]  W. Brouwer,et al.  Simulated driving in obstructive sleep apnoea–hypopnoea; effects of oral appliances and continuous positive airway pressure , 2007, Sleep and Breathing.

[74]  Joseph M. Galea,et al.  Disruption of the Dorsolateral Prefrontal Cortex Facilitates the Consolidation of Procedural Skills , 2010, Journal of Cognitive Neuroscience.

[75]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Sunbin Song,et al.  Perceptual sequence learning in a serial reaction time task , 2008, Experimental Brain Research.

[77]  Ilona Kovács,et al.  Sleep dependent learning in contour integration , 2007 .

[78]  William L. Gross,et al.  Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task. , 2007, Learning & memory.

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

[80]  D. Howard,et al.  Implicit sequence learning: effects of level of structure, adult age, and extended practice. , 2004, Psychology and aging.

[81]  Sunbin Song,et al.  Consciousness and the consolidation of motor learning , 2009, Behavioural Brain Research.

[82]  Eric Soetens,et al.  Perceptual or motor learning in SRT tasks with complex sequence structures , 2006, Psychological research.

[83]  Leslie G. Ungerleider,et al.  Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning , 2009, Experimental Brain Research.

[84]  Walter Paulus,et al.  Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human , 2004, Neuropsychologia.

[85]  A. Reber Implicit learning and tacit knowledge , 1993 .

[86]  C B Cave,et al.  Memory: organization of brain systems and cognition. , 1993, Cold Spring Harbor symposia on quantitative biology.

[87]  D Broadbent,et al.  Implicit and explicit knowledge bases in artificial grammar learning. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

[88]  P. Frensch,et al.  Effects of presentation rate and individual differences in short-term memory capacity on an indirect measure of serial learning , 1994, Memory & cognition.

[89]  R. Stickgold,et al.  Sleep-Dependent Learning and Memory Consolidation , 2004, Neuron.

[90]  I. Bennett,et al.  Age-related differences in implicit learning of subtle third-order sequential structure. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[91]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[92]  D. Howard,et al.  Age differences in learning serial patterns: direct versus indirect measures. , 1989, Psychology and aging.

[93]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

[94]  Roberto Cabeza,et al.  Age-related dedifferentiation of learning systems: an fMRI study of implicit and explicit learning , 2011, Neurobiology of Aging.

[95]  Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks , 2002, Experimental Brain Research.

[96]  Leslie G. Ungerleider,et al.  Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. , 2008, Sleep.

[97]  Dileep George,et al.  Sequence memory for prediction, inference and behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[98]  J. Born,et al.  Sleep forms memory for finger skills , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[99]  G. Remillard Pure perceptual-based sequence learning: a role for visuospatial attention. , 2009, Journal of experimental psychology. Learning, memory, and cognition.

[100]  Jennifer Romano Bergstrom,et al.  Enhanced Implicit Sequence Learning in College‐age Video Game Players and Musicians , 2012 .

[101]  Gustavo A. Vázquez,et al.  Implicit sequence learning and contextual cueing do not compete for central cognitive resources. , 2011, Journal of experimental psychology. Human perception and performance.

[102]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

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

[104]  Michael J. Frank,et al.  When Memory Fails, Intuition Reigns , 2006, Psychological science.

[105]  Karolina Janacsek,et al.  Interference between Sentence Processing and Probabilistic Implicit Sequence Learning , 2011, PloS one.

[106]  G. Remillard Pure perceptual-based sequence learning. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[107]  Thomas Goschke,et al.  Implicit learning of perceptual and motor sequences: Evidence for independent learning systems. , 1998 .

[108]  L. Squire,et al.  The structure and organization of memory. , 1993, Annual review of psychology.

[109]  Gilbert Remillard,et al.  Implicit Learning of Second-, Third-, and Fourth-Order Adjacent and Nonadjacent Sequential Dependencies , 2008, Quarterly journal of experimental psychology.

[110]  D. Willingham Systems of Memory in the Human Brain , 1997, Neuron.

[111]  N. Mackintosh,et al.  Implicit learning as an ability , 2010, Cognition.

[112]  E. Robertson From Creation to Consolidation: A Novel Framework for Memory Processing , 2009, PLoS biology.

[113]  Richard I. Ivry,et al.  Attention and structure in sequence learning. , 1990 .

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

[115]  L. Boyd,et al.  Sleep to learn after stroke: Implicit and explicit off-line motor learning , 2009, Neuroscience Letters.

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

[117]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[118]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[119]  R. Stickgold,et al.  Dissociable stages of human memory consolidation and reconsolidation , 2003, Nature.

[120]  Karolina Janacsek,et al.  The dynamics of implicit skill consolidation in young and elderly adults. , 2011, The journals of gerontology. Series B, Psychological sciences and social sciences.