Offline consolidation of procedural skill learning is enhanced by negative emotional content

It is now well established that both procedural skills and episodic memories consolidate across periods of offline retention, and most particularly across periods of sleep. Such consolidation has been demonstrated to be more marked for emotional than for neutral episodes, but the interaction between emotionality and the offline consolidation of procedural skills has yet to be investigated. Here, we address this issue by examining the impact of an emotional background context at encoding upon the subsequent consolidation of mirror tracing, a well-studied procedural skill. We also consider the importance of sleep for such consolidation by manipulating the retention interval (over a day, overnight, or over 24 h containing normal sleep). Our data show significantly greater offline improvements in the accuracy of mirror tracing when negative emotional content is present during the training phase when compared to when neutral or positive content is present. Furthermore, consolidation across a night of sleep is associated with faster and more accurate performance than consolidation across a day of wakefulness. These novel findings show that the emotional context in which a procedural skill is learned can impact upon subsequent offline consolidation.

[1]  J. Born,et al.  Effects of Early and Late Nocturnal Sleep on Declarative and Procedural Memory , 1997, Journal of Cognitive Neuroscience.

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

[3]  R. Dolan,et al.  Emotion, Decision Making, and the Amygdala , 2008, Neuron.

[4]  J. Aldenhoff,et al.  Impairment of visuospatial memory is associated with decreased slow wave sleep in schizophrenia. , 2004, Journal of psychiatric research.

[5]  J. Born,et al.  Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Edwin M Robertson,et al.  Understanding Consolidation through the Architecture of Memories , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[7]  M. Walker The Role of Sleep in Cognition and Emotion , 2009, Annals of the New York Academy of Sciences.

[8]  J. Adams Historical review and appraisal of research on the learning, retention, and transfer of human motor skills. , 1987 .

[9]  I. Heuser,et al.  The Relationship Between REM Sleep and Memory Consolidation in Old Age and Effects of Cholinergic Medication , 2007, Biological Psychiatry.

[10]  Robert Stickgold,et al.  Sleep Preferentially Enhances Memory for Emotional Components of Scenes , 2008, Psychological science.

[11]  Elizabeth A. Phelps,et al.  How arousal modulates memory: Disentangling the effects of attention and retention , 2004, Cognitive, affective & behavioral neuroscience.

[12]  M. Walker,et al.  A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. , 2011, Cerebral cortex.

[13]  Manuel Schabus,et al.  Sleep-Related Hippocampo-Cortical Interplay during Emotional Memory Recollection , 2007, PLoS biology.

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

[15]  Turhan Canli,et al.  Individual differences in emotion processing , 2004, Current Opinion in Neurobiology.

[16]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[17]  Masako Tamaki,et al.  Fast sleep spindle (13-15 hz) activity correlates with sleep-dependent improvement in visuomotor performance. , 2008, Sleep.

[18]  J. D. McGaugh,et al.  Role of adrenal stress hormones in forming lasting memories in the brain , 2002, Current Opinion in Neurobiology.

[19]  E Levonian,et al.  Retention over time in relation to arousal during learning: an explantation of discrepant results. , 1972, Acta psychologica.

[20]  Stuart M. Fogel,et al.  Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems , 2007, Behavioural Brain Research.

[21]  L H Staib,et al.  Gender differences in cognitive and neural correlates of remembrance of emotional words. , 2001, Psychopharmacology bulletin.

[22]  Ruth O'Hara,et al.  Memory before and after sleep in patients with moderate obstructive sleep apnea. , 2009, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[23]  Ralph Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  E. Phelps,et al.  Arousal-Mediated Memory Consolidation: Role of the Medial Temporal Lobe in Humans , 1998 .

[25]  Kai Spiegelhalder,et al.  Sleep‐related memory consolidation in primary insomnia , 2011, Journal of sleep research.

[26]  Bruce S. McEwen,et al.  Stress, memory and the amygdala , 2009, Nature Reviews Neuroscience.

[27]  R. F. Westbrook,et al.  Fear Conditioning and Long‐term Potentiation in the Amygdala , 2008, Annals of the New York Academy of Sciences.

[28]  Larry Cahill,et al.  The influence of sex versus sex-related traits on long-term memory for gist and detail from an emotional story , 2004, Consciousness and Cognition.

[29]  Edwin M. Robertson,et al.  Motor sequence consolidation: constrained by critical time windows or competing components , 2007, Experimental Brain Research.

[30]  R. Buckner,et al.  REM Sleep, Prefrontal Theta, and the Consolidation of Human Emotional Memory , 2008, Cerebral cortex.

[31]  M. Walker,et al.  Sleep deprivation impairs the accurate recognition of human emotions. , 2010, Sleep.

[32]  Stephen Maren,et al.  Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats , 2008, The European journal of neuroscience.

[33]  J. Born,et al.  Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory , 2004, The Journal of Neuroscience.

[34]  J. Born,et al.  Effects of early and late nocturnal sleep on priming and spatial memory. , 1999, Psychophysiology.

[35]  A. Prehn-Kristensen,et al.  Sleep in children enhances preferentially emotional declarative but not procedural memories. , 2009, Journal of experimental child psychology.

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

[37]  L. Cahill,et al.  Neurobiological mechanisms of emotionally influenced, long-term memory. , 2000, Progress in brain research.

[38]  Alvaro Pascual-Leone,et al.  Current concepts in procedural consolidation , 2004, Nature Reviews Neuroscience.

[39]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[40]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[41]  Y. Humeau,et al.  Amygdala Inhibitory Circuits and the Control of Fear Memory , 2009, Neuron.

[42]  Larry Cahill,et al.  Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding , 2003, Neurobiology of Learning and Memory.

[43]  I. Heuser,et al.  Declarative and procedural memory consolidation during sleep in patients with borderline personality disorder. , 2008, Journal of psychiatric research.

[44]  R. Morecraft,et al.  Convergence of Limbic Input to the Cingulate Motor Cortex in the Rhesus Monkey , 1998, Brain Research Bulletin.

[45]  近間 正典 Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1998 .

[46]  K. Ochsner,et al.  Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. , 2000, Journal of experimental psychology. General.

[47]  J. Born,et al.  Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. , 2001, Learning & memory.

[48]  S. Haber Integrating Cognition and Motivation into the Basal Ganglia Pathways of Action , 2003 .

[49]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[50]  Daniel B. Willingham,et al.  Intact mirror-tracing and impaired rotary-pursuit skill learning in patients with Huntington's disease: evidence for dissociable memory systems in skill learning. , 1997, Neuropsychology.

[51]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

[52]  L. Cosmides From : The Cognitive Neurosciences , 1995 .

[53]  L. Heimer,et al.  Ventral striatum and ventral pallidum Components of the motor system? , 1982, Trends in Neurosciences.

[54]  J. Born,et al.  Dexamethasone blocks sleep induced improvement of declarative memory , 1999, Psychoneuroendocrinology.

[55]  X. Morandi,et al.  The subthalamic nucleus is a key-structure of limbic basal ganglia functions. , 2009, Medical hypotheses.

[56]  J. Aldenhoff,et al.  Effects of daytime naps on procedural and declarative memory in patients with schizophrenia. , 2010, Journal of psychiatric research.

[57]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

[59]  J. Mixter Fast , 2012 .

[60]  J. Hobson,et al.  Visual discrimination learning requires sleep after training , 2000, Nature Neuroscience.

[61]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[62]  Manuel Schabus,et al.  Sleep spindle‐related activity in the human EEG and its relation to general cognitive and learning abilities , 2006, The European journal of neuroscience.

[63]  J. Price,et al.  Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks , 2000, The Journal of comparative neurology.

[64]  S. Kaplan,et al.  Paired-associate learning as a function of arousal and interpolated interval. , 1963, Journal of experimental psychology.

[65]  Robert D. Tarte,et al.  Memory Storage as a Function of Arousal and Time with Homogeneous and Heterogeneous Lists , 1963 .

[66]  M. Hallett,et al.  Motor learning in patients with cerebellar dysfunction. , 1990, Brain : a journal of neurology.

[67]  L. Rabin,et al.  Gender differences in implicit and explicit memory for affective passages , 2004, Brain and Cognition.

[68]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

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

[70]  R. Dolan,et al.  Encoding of emotional memories depends on amygdala and hippocampus and their interactions , 2004, Nature Neuroscience.

[71]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[72]  B. Milner Physiologie de l'Hippocampe: Colloque International, No. 107, Editions du Centre National de la Recherche Scientifique, Paris, 1962. 512 pp. 58NF , 1965 .

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

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

[75]  A. Thierry,et al.  Motor and Cognitive Functions of the Prefrontal Cortex , 1994, Research and Perspectives in Neurosciences.

[76]  H. Groenewegen,et al.  Anatomical Relationships Between the Prefrontal Cortex and the Basal Ganglia in the Rat , 1994 .

[77]  J. Aldenhoff,et al.  Visual declarative memory is associated with non-rapid eye movement sleep and sleep cycles in patients with chronic non-restorative sleep. , 2007, Sleep medicine.

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

[79]  Steven Laureys,et al.  Sleep and Motor Skill Learning , 2002, Neuron.

[80]  Rachel J. Garoff-Eaton,et al.  Memory for Specific Visual Details can be Enhanced by Negative Arousing Content. , 2006 .

[81]  J D Gabrieli,et al.  Intact acquisition and long-term retention of mirror-tracing skill in Alzheimer's disease and in global amnesia. , 1993, Behavioral neuroscience.

[82]  B. Feige,et al.  Impaired sleep-related memory consolidation in primary insomnia--a pilot study. , 2006, Sleep.