Susceptibility to Declarative Memory Interference is Pronounced in Primary Insomnia

Sleep has been shown to stabilize memory traces and to protect against competing interference in both the procedural and declarative memory domain. Here, we focused on an interference learning paradigm by testing patients with primary insomnia (N = 27) and healthy control subjects (N = 21). In two separate experimental nights with full polysomnography it was revealed that after morning interference procedural memory performance (using a finger tapping task) was not impaired in insomnia patients while declarative memory (word pair association) was decreased following interference. More specifically, we demonstrate robust associations of central sleep spindles (in N3) with motor memory susceptibility to interference as well as (cortically more widespread) fast spindle associations with declarative memory susceptibility. In general the results suggest that insufficient sleep quality does not necessarily show up in worse overnight consolidation in insomnia but may only become evident (in the declarative memory domain) when interference is imposed.

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

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

[3]  S. Ancoli-Israel,et al.  Daytime consequences and correlates of insomnia in the United States: results of the 1991 National Sleep Foundation Survey. II. , 1999, Sleep.

[4]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

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

[6]  C. Degueldre,et al.  Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness , 2006, PLoS biology.

[7]  A. Schlögl,et al.  An E-Health Solution for Automatic Sleep Classification according to Rechtschaffen and Kales: Validation Study of the Somnolyzer 24 × 7 Utilizing the Siesta Database , 2005, Neuropsychobiology.

[8]  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.

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

[10]  R. Vertes,et al.  Memory Consolidation in Sleep Dream or Reality , 2004, Neuron.

[11]  S. Drummond,et al.  Discrepancy between subjective symptomatology and objective neuropsychological performance in insomnia. , 2007, Sleep.

[12]  C. Reynolds,et al.  Epidemiological and clinical relevance of insomnia diagnosis algorithms according to the DSM-IV and the International Classification of Sleep Disorders (ICSD). , 2009, Sleep medicine.

[13]  Axel Cleeremans,et al.  Filling one gap by creating another: Memory stabilization is not all-or-nothing, either , 2005 .

[14]  Jerome M. Siegel,et al.  The REM Sleep-Memory Consolidation Hypothesis , 2001, Science.

[15]  G. Rauchs,et al.  The relationships between memory systems and sleep stages , 2005, Journal of sleep research.

[16]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[17]  Manuel Schabus,et al.  Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep , 2007, Proceedings of the National Academy of Sciences.

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

[19]  R. Stickgold,et al.  Sleep-dependent learning and motor-skill complexity. , 2004, Learning & memory.

[20]  D. Fabó,et al.  Overnight verbal memory retention correlates with the number of sleep spindles , 2005, Neuroscience.

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

[22]  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.

[23]  J. Born,et al.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. , 2007, Brain : a journal of neurology.

[24]  Jan Born,et al.  Impaired Declarative Memory Consolidation During Sleep in Patients With Primary Insomnia: Influence of Sleep Architecture and Nocturnal Cortisol Release , 2006, Biological Psychiatry.

[25]  P. Maquet,et al.  Early boost and slow consolidation in motor skill learning. , 2006, Learning & memory.

[26]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[27]  R. Bootzin,et al.  Derivation of research diagnostic criteria for insomnia: report of an American Academy of Sleep Medicine Work Group. , 2004, Sleep.

[28]  J. Walsh,et al.  Clinical and socioeconomic correlates of insomnia. , 2004, The Journal of clinical psychiatry.

[29]  J. Csicsvari,et al.  Communication between neocortex and hippocampus during sleep in rodents , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  David F. Dinges,et al.  Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations , 1985 .

[31]  N. Rogers,et al.  Searching for the daytime impairments of primary insomnia. , 2010, Sleep medicine reviews.

[32]  Hans P A Van Dongen,et al.  Chronic Insomnia and Daytime Functioning: An Ambulatory Assessment , 2007, Behavioral sleep medicine.

[33]  J. Mixter.  Fast , 2012 .

[34]  I. Wilhelm,et al.  The whats and whens of sleep-dependent memory consolidation. , 2009, Sleep medicine reviews.

[35]  Manuel Schabus,et al.  Still missing some significant ingredients. , 2009, Sleep.

[36]  J. Broman,et al.  Subjective and Objective Performance in Patients with Persistent Insomnia , 1992 .

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

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

[39]  Justin C. Hulbert,et al.  Interfering with Theories of Sleep and Memory: Sleep, Declarative Memory, and Associative Interference , 2006, Current Biology.

[40]  K. Paller,et al.  Memory stabilization with targeted reactivation during human slow-wave sleep , 2012, Proceedings of the National Academy of Sciences.

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

[42]  P. Maquet,et al.  Repetitive transcranial magnetic stimulation over the primary motor cortex disrupts early boost but not delayed gains in performance in motor sequence learning , 2008, The European journal of neuroscience.

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

[44]  G. Rauchs,et al.  Consolidation of strictly episodic memories mainly requires rapid eye movement sleep. , 2004, Sleep.

[45]  C. Morin,et al.  Insomnia and daytime cognitive performance: a meta-analysis. , 2012, Sleep medicine reviews.

[46]  C. Morin,et al.  Epidemiology of insomnia: prevalence, self-help treatments, consultations, and determinants of help-seeking behaviors. , 2006, Sleep medicine.

[47]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[48]  Björn Rasch,et al.  Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory , 2009, Nature Neuroscience.

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

[50]  S. Kyle,et al.  Towards an improved neuropsychology of poor sleep? , 2008, Sleep.

[51]  Matthew P Walker,et al.  A refined model of sleep and the time course of memory formation. , 2005, The Behavioral and brain sciences.

[52]  J. Born,et al.  Declarative memory consolidation: mechanisms acting during human sleep. , 2004, Learning & memory.

[53]  E. Hoddes,et al.  The history and use of the Stanford sleepiness scale , 1971 .

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

[55]  Manuel Schabus,et al.  Sleep spindles and their significance for declarative memory consolidation. , 2004, Sleep.

[56]  Stuart M Fogel,et al.  Learning‐dependent changes in sleep spindles and Stage 2 sleep , 2006, Journal of sleep research.

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

[58]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[59]  Mario Rosanova,et al.  Pattern-Specific Associative Long-Term Potentiation Induced by a Sleep Spindle-Related Spike Train , 2005, The Journal of Neuroscience.

[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.  The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats , 2009, The European journal of neuroscience.

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