Electrical Source Imaging of Sleep Spindles

To identify and compare cortical source generators of slow and fast sleep spindles in healthy subjects, electroencephalographic (EEG) signals were obtained from 256 channels, and sources on neuroanatomical Montreal Neurological Institute (MNI) space estimated with low-resolution brain electromagnetic tomography analysis (LORETA). Spindle activity was recorded in 18 healthy volunteers during daytime napping. Because of lack of sleep or excessive artifacts, data from 13 subjects were analyzed off-line. Spindles were visually scored, marked, and bandpass filtered (slow 10-12 Hz or fast 12-14 Hz). EEG was segmented on the marker, and segments separately averaged. LORETA projected cortical sources on the MNI brain. Maximal intra- and inter-individual intensities were compared using the Wilcoxon test (P< .05) and cortical sources distribution compared using a χ2 test. Two to three slow spindles generators were consistently identified in frontal lobes, with additional sources in parietal and limbic lobes in half cases. Fast spindles had multiple temporo-parietal sources, with an inconstant frontal source. Inter-individual (P = 0.44), and intra-individual (P = 0.09 slow and P = 0.10 fast spindles) source intensities were comparable. Slow spindles sources were preferentially concentrated over frontal cortices in comparison with fast spindles (P = 0.0009). Our results demonstrate multiple, synchronous, and equipotent spindles cortical generators in healthy subjects, with more anterior generators for slow spindles.

[1]  A. Loomis,et al.  POTENTIAL RHYTHMS OF THE CEREBRAL CORTEX DURING SLEEP. , 1935, Science.

[2]  W. Martens,et al.  Human sleep spindle characteristics after sleep deprivation , 2003, Clinical Neurophysiology.

[3]  J. Born,et al.  Sleep to Remember , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  P. Manganotti,et al.  A multimodal imaging approach to the evaluation of post-traumatic epilepsy , 2012, Magnetic Resonance Materials in Physics, Biology and Medicine.

[5]  Norman Tepley,et al.  Cortical locations of maximal spindle activity: magnetoencephalography (MEG) study , 2009, Journal of sleep research.

[6]  H. Lüders,et al.  EEG source imaging in epilepsy—practicalities and pitfalls , 2012, Nature Reviews Neurology.

[7]  M. Bertini,et al.  Effect of slow-wave sleep deprivation on topographical distribution of spindles , 2000, Behavioural Brain Research.

[8]  Helmut Laufs,et al.  'Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study'--its limitations and an alternative approach. , 2007, Brain : a journal of neurology.

[9]  F. Gibbs,et al.  Atlas of electroencephalography , 1941 .

[10]  Patrick Van Bogaert,et al.  Neuronal networks in children with continuous spikes and waves during slow sleep. , 2011, Brain : a journal of neurology.

[11]  Tanya I. Baker,et al.  Interactions between Core and Matrix Thalamocortical Projections in Human Sleep Spindle Synchronization , 2012, The Journal of Neuroscience.

[12]  G. Tononi,et al.  Source modeling sleep slow waves , 2009, Proceedings of the National Academy of Sciences.

[13]  M. Steriade,et al.  Sleep Oscillations Developing into Seizures in Corticothalamic Systems , 2003, Epilepsia.

[14]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[15]  Lino Nobili,et al.  Hippocampal Sleep Features: Relations to Human Memory Function , 2012, Front. Neur..

[16]  Christoph M. Michel,et al.  Towards the utilization of EEG as a brain imaging tool , 2012, NeuroImage.

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

[18]  Liborio Parrino,et al.  Cyclic alternating pattern (CAP) and epilepsy during sleep: how a physiological rhythm modulates a pathological event , 2000, Clinical Neurophysiology.

[19]  Yuko Urakami,et al.  Relationships Between Sleep Spindles and Activities of Cerebral Cortex as Determined by Simultaneous EEG and MEG Recording , 2008, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[20]  G. Tononi,et al.  Sex-related differences in sleep slow wave activity in major depressive disorder: a high-density EEG investigation , 2012, BMC Psychiatry.

[21]  P. Achermann,et al.  Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. , 1997, Electroencephalography and clinical neurophysiology.

[22]  M. Steriade.  The corticothalamic system in sleep. , 2003, Frontiers in bioscience : a journal and virtual library.

[23]  Julie Carrier,et al.  Topography of age-related changes in sleep spindles , 2013, Neurobiology of Aging.

[24]  P. Manganotti,et al.  Slow spindles’ cortical generators overlap with the epileptogenic zone in temporal epileptic patients: An electrical source imaging study , 2013, Clinical Neurophysiology.

[25]  H Spekreijse,et al.  The extrastriate generators of the EP to checkerboard onset. A source localization approach. , 1991, Electroencephalography and clinical neurophysiology.

[26]  Maria Concetta Pellicciari,et al.  Effect of total sleep deprivation on the landmarks of stage 2 sleep , 2003, Clinical Neurophysiology.

[27]  H. Merica,et al.  The Neuronal Transition Probability (NTP) Model for the Dynamic Progression of Non-REM Sleep EEG: The Role of the Suprachiasmatic Nucleus , 2011, PloS one.

[28]  Jean-François Gagnon,et al.  Sleep and quantitative EEG in neurodegenerative disorders. , 2004, Journal of psychosomatic research.

[29]  Jan Born,et al.  Slow oscillations orchestrating fast oscillations and memory consolidation. , 2011, Progress in brain research.

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

[31]  Manuel Schabus,et al.  The Fate of Incoming Stimuli during NREM Sleep is Determined by Spindles and the Phase of the Slow Oscillation , 2011, Front. Neur..

[32]  S. Sarasso,et al.  Electrophysiological traces of visuomotor learning and their renormalization after sleep , 2011, Clinical Neurophysiology.

[33]  E. Halgren,et al.  Emergence of synchronous EEG spindles from asynchronous MEG spindles , 2011, Human brain mapping.

[34]  D Lehmann,et al.  Sleep deprivation: effect on sleep stages and EEG power density in man. , 1981, Electroencephalography and clinical neurophysiology.

[35]  C. Michel,et al.  Propagation of Interictal Epileptiform Activity Can Lead to Erroneous Source Localizations: A 128-Channel EEG Mapping Study , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  E. Halgren,et al.  Magnetoencephalography demonstrates multiple asynchronous generators during human sleep spindles. , 2010, Journal of neurophysiology.

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

[38]  B. Dan,et al.  A neurophysiological perspective on sleep and its maturation. , 2006, Developmental medicine and child neurology.

[39]  G Klösch,et al.  Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex , 2001, Neuroscience.

[40]  S. Chokroverty,et al.  The visual scoring of sleep in adults. , 2007, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

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

[42]  Claudio Pollo,et al.  Electrical source imaging for presurgical focus localization in epilepsy patients with normal MRI , 2010, Epilepsia.

[43]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[44]  Claudio Pollo,et al.  Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients , 2011, Brain : a journal of neurology.

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

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

[47]  A. Wirz-Justice,et al.  Homeostatic control of slow-wave and spindle frequency activity during human sleep: effect of differential sleep pressure and brain topography. , 2002, Cerebral cortex.

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

[49]  S. Daan,et al.  EEG Power Density during Nap Sleep: Reflection of an Hourglass Measuring the Duration of Prior Wakefulness , 1987, Journal of biological rhythms.

[50]  I. Fried,et al.  Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings , 2011, The Journal of Neuroscience.

[51]  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.

[52]  J. Parvizi,et al.  Functional MRI of sleep spindles and K-complexes , 2012, Clinical Neurophysiology.

[53]  T. Sejnowski,et al.  Spatiotemporal Patterns of Spindle Oscillations in Cortex and Thalamus , 1997, The Journal of Neuroscience.

[54]  J. Born,et al.  Slow-wave sleep and the consolidation of long-term memory , 2010, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[55]  M. Kryger,et al.  Principles and Practice of Sleep Medicine , 1989 .