Local sleep spindle modulations in relation to specific memory cues

Sleep spindles have been connected to memory processes in various ways. In addition, spindles appear to be modulated at the local cortical network level. We investigated whether cueing specific memories during sleep leads to localized spindle modulations in humans. During learning of word-location associations, words presented in the left and right visual hemifields were paired with different odors. By presenting a single odor during a subsequent nap, we aimed to selectively reactivate a subset of the studied material in sleeping subjects. During sleep, we observed topographically restricted spindle responses to memory cues, suggesting successful reactivation of specific memory traces. In particular, we found higher amplitude and greater incidence of fast spindles over posterior brain areas involved in visuospatial processing, contralateral to the visual field being cued. These results suggest that sleep spindles in different cortical areas reflect the reprocessing of specific memory traces.

[1]  J. Schoffelen,et al.  Dissociated α-band modulations in the dorsal and ventral visual pathways in visuospatial attention and perception. , 2014, Cerebral cortex.

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

[3]  Manuel Schabus,et al.  Susceptibility to Declarative Memory Interference is Pronounced in Primary Insomnia , 2013, PloS one.

[4]  M. Deschenes,et al.  The deafferented reticular thalamic nucleus generates spindle rhythmicity. , 1987, Journal of neurophysiology.

[5]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

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

[7]  G. Tononi,et al.  Local sleep in awake rats , 2011, Nature.

[8]  Monika Schönauer,et al.  Strengthening Procedural Memories by Reactivation in Sleep , 2014, Journal of Cognitive Neuroscience.

[9]  Maxime Bonjean,et al.  Corticothalamic Feedback Controls Sleep Spindle Duration In Vivo , 2011, The Journal of Neuroscience.

[10]  Atsuko Takashima,et al.  Sleep directly following learning benefits consolidation of spatial associative memory. , 2008, Learning & memory.

[11]  G. Tononi,et al.  Reduced sleep spindle activity in schizophrenia patients. , 2007, The American journal of psychiatry.

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

[13]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[14]  Guillén Fernández,et al.  Shift from Hippocampal to Neocortical Centered Retrieval Network with Consolidation , 2009, The Journal of Neuroscience.

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

[16]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

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

[18]  Matthew P Walker,et al.  The role of sleep in directed forgetting and remembering of human memories. , 2011, Cerebral cortex.

[19]  J. Born,et al.  Learning-Dependent Increases in Sleep Spindle Density , 2002, The Journal of Neuroscience.

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

[21]  Mark G. Stokes,et al.  Attention Modulates Maintenance of Representations in Visual Short-term Memory , 2012, Journal of Cognitive Neuroscience.

[22]  Joel L. Voss,et al.  Strengthening Individual Memories by Reactivating Them During Sleep , 2009, Science.

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

[24]  Björn Rasch,et al.  Reactivating Memories during Sleep by Odors: Odor Specificity and Associated Changes in Sleep Oscillations , 2014, Journal of Cognitive Neuroscience.

[25]  I. Fried,et al.  Regional Slow Waves and Spindles in Human Sleep , 2011, Neuron.

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

[27]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

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

[29]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[30]  Sean L. Hill,et al.  The Sleep Slow Oscillation as a Traveling Wave , 2004, The Journal of Neuroscience.

[31]  J. Born,et al.  Labile or stable: opposing consequences for memory when reactivated during waking and sleep , 2011, Nature Neuroscience.

[32]  T. Sejnowski,et al.  Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep , 2011, Proceedings of the National Academy of Sciences.

[33]  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.

[34]  Anita Lüthi,et al.  Sleep Spindles , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[35]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[36]  Ninad Gujar,et al.  Sleep-Dependent Facilitation of Episodic Memory Details , 2011, PloS one.

[37]  G. Tononi,et al.  TMS-Induced Cortical Potentiation during Wakefulness Locally Increases Slow Wave Activity during Sleep , 2007, PloS one.

[38]  T. Vilis,et al.  Remapping the remembered target location for anti-saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

[39]  P. Cotton,et al.  Contralateral visual hemifield representations in the human pulvinar nucleus. , 2007, Journal of neurophysiology.

[40]  P. Anderer,et al.  Topographic distribution of sleep spindles in young healthy subjects , 1997, Journal of sleep research.

[41]  Ole Jensen,et al.  Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli , 2011, Journal of Cognitive Neuroscience.

[42]  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.

[43]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[44]  Eric W. Gobel,et al.  Cued Memory Reactivation During Sleep Influences Skill Learning , 2012, Nature Neuroscience.

[45]  Leslie G. Ungerleider,et al.  Fast and slow spindle involvement in the consolidation of a new motor sequence , 2011, Behavioural Brain Research.

[46]  Carlyle T. Smith,et al.  The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation , 2011, Neuroscience & Biobehavioral Reviews.

[47]  Roy Cox,et al.  Involvement of spindles in memory consolidation is slow wave sleep-specific. , 2012, Learning & memory.

[48]  G. Tononi,et al.  Local sleep and learning , 2004, Nature.

[49]  Jan Born,et al.  Fine‐tuned coupling between human parahippocampal ripples and sleep spindles , 2011, The European journal of neuroscience.

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

[51]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

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

[53]  J. Born,et al.  Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations , 2012, Neurobiology of Learning and Memory.

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

[55]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[56]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[57]  W P Medendorp,et al.  Reorganization of oscillatory activity in human parietal cortex during spatial updating. , 2013, Cerebral cortex.

[58]  Daniel Bendor,et al.  Biasing the content of hippocampal replay during sleep , 2012, Nature Neuroscience.

[59]  Lucia M. Talamini,et al.  Time, Not Sleep, Unbinds Contexts from Item Memory , 2014, PloS one.

[60]  M. Carskadon,et al.  Minimal olfactory perception during sleep: why odor alarms will not work for humans. , 2004, Sleep.

[61]  K. Petersson,et al.  Memory trace stabilization leads to large-scale changes in the retrieval network: a functional MRI study on associative memory. , 2007, Learning & memory.

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