Topography of age-related changes in sleep spindles

Aging induces multiple changes to sleep spindles, which may hinder their alleged functional role in memory and sleep protection mechanisms. Brain aging in specific cortical regions could affect the neural networks underlying spindle generation, yet the topography of these age-related changes is currently unknown. In the present study, we analyzed spindle characteristics in 114 healthy volunteers aged between 20 and 73 years over 5 anteroposterior electroencephalography scalp derivations. Spindle density, amplitude, and duration were higher in young subjects than in middle-aged and elderly subjects in all derivations, but the topography of age effects differed drastically. Age-related decline in density and amplitude was more prominent in anterior derivations, whereas duration showed a posterior prominence. Age groups did not differ in all-night spindle frequency for any derivation. These results show that age-related changes in sleep spindles follow distinct topographical patterns that are specific to each spindle characteristic. This topographical specificity may provide a useful biomarker to localize age-sensitive changes in underlying neural systems during normal and pathological aging.

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

[2]  P Achermann,et al.  Power and coherence of sleep spindle frequency activity following hemispheric stroke. , 2002, Brain : a journal of neurology.

[3]  M. Ferrara,et al.  Sleep spindles: an overview. , 2003, Sleep medicine reviews.

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

[5]  D. Contreras,et al.  Cortically-induced coherence of a thalamic-generated oscillation , 1999, Neuroscience.

[6]  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.

[7]  Brahim Selmaoui,et al.  Effects of caffeine on daytime recovery sleep: A double challenge to the sleep-wake cycle in aging. , 2009, Sleep medicine.

[8]  J. Carrier,et al.  Effects of Caffeine are more Marked on Daytime Recovery Sleep than on Nocturnal Sleep , 2007, Neuropsychopharmacology.

[9]  J. Allan Hobson,et al.  A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects: A. Rechtschaffen and A. Kales (Editors). (Public Health Service, U.S. Government Printing Office, Washington, D.C., 1968, 58 p., $4.00) , 1969 .

[10]  G. Fein,et al.  Sleep spindles in normal elderly: comparison with young adult patterns and relation to nocturnal awakening, cognitive function and brain atrophy. , 1986, Electroencephalography and clinical neurophysiology.

[11]  R. Rissman,et al.  GABAA receptors in aging and Alzheimer’s disease , 2007, Journal of neurochemistry.

[12]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[13]  Julie Carrier,et al.  Aging Worsens the Effects of Sleep Deprivation on Postural Control , 2011, PloS one.

[14]  S. Moshé,et al.  Age- and gender-related differences in GABAA receptor-mediated postsynaptic currents in GABAergic neurons of the substantia nigra reticulata in the rat , 2009, Neuroscience.

[15]  A. Beck.  The Beck Depression Inventory , 1978 .

[16]  K. Crowley,et al.  The effects of normal aging on sleep spindle and K-complex production , 2002, Clinical Neurophysiology.

[17]  N. Akaike,et al.  Developmental changes of GABAA receptor-chloride channels in rat Meynert neurons , 1998, Brain Research.

[18]  Faith M. Gunning-Dixon,et al.  Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume , 2004, Neurobiology of Aging.

[19]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

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

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

[22]  R. Vasko,et al.  Muscle artifacts in the sleep EEG: Automated detection and effect on all‐night EEG power spectra , 1996, Journal of sleep research.

[23]  M. Steriade.  Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[24]  A. Borbély,et al.  All‐night dynamics of the human sleep EEG , 1993, Journal of sleep research.

[25]  S. Yamaguchi,et al.  Gender effects on age-related changes in brain structure. , 2000, AJNR. American journal of neuroradiology.

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

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

[28]  Domien G. M. Beersma,et al.  All night spectral analysis of EEG sleep in young adult and middle-aged male subjects , 1989, Neurobiology of Aging.

[29]  T. J. Sejnowski,et al.  Self–sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials , 1999, Nature Neuroscience.

[30]  A. Apkarian,et al.  Aging alters the multichemical networking profile of the human brain: an in vivo1H‐MRS study of young versus middle‐aged subjects , 2001, Journal of neurochemistry.

[31]  K. Walhovd,et al.  Structural Brain Changes in Aging: Courses, Causes and Cognitive Consequences , 2010, Reviews in the neurosciences.

[32]  T H Monk,et al.  The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20-60 years old). , 2001, Psychophysiology.

[33]  A. Dale,et al.  High consistency of regional cortical thinning in aging across multiple samples. , 2009, Cerebral cortex.

[34]  J. Montplaisir,et al.  Sleep spindle characteristics in healthy subjects of different age groups , 2001, Clinical Neurophysiology.

[35]  Bruce Fischl,et al.  Regional white matter volume differences in nondemented aging and Alzheimer's disease , 2009, NeuroImage.

[36]  A. Toga,et al.  Mapping Changes in the Human Cortex throughout the Span of Life , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[38]  M Steriade,et al.  Sleep oscillations and their blockage by activating systems. , 1994, Journal of psychiatry & neuroscience : JPN.

[39]  McGeer Pl,et al.  Aging and neurotransmitter systems. , 1980 .

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

[41]  J. Carrier,et al.  Age‐related modifications of NREM sleep EEG: from childhood to middle age , 2001, Journal of sleep research.

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

[43]  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.

[44]  Abimbola Farinde,et al.  The Beck Depression Inventory , 2013 .

[45]  H. Uylings,et al.  Thalamic volume predicts performance on tests of cognitive speed and decreases in healthy aging. A magnetic resonance imaging-based volumetric analysis. , 2001, Brain research. Cognitive brain research.

[46]  Terrence J. Sejnowski,et al.  Contribution of intrinsic and synaptic factors in the desynchronization of thalamic oscillatory activity , 2001 .

[47]  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.

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

[49]  Alan C. Evans,et al.  A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. , 2004, Cerebral cortex.

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

[51]  Derk-Jan Dijk,et al.  Attenuated amplitude of circadian and sleep-dependent modulation of electroencephalographic sleep spindle characteristics in elderly human subjects , 1999, Neuroscience Letters.

[52]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[53]  Adolf Pfefferbaum,et al.  Effects of age and sex on volumes of the thalamus, pons, and cortex , 2004, Neurobiology of Aging.

[54]  J. R. Smith,et al.  Sleep spindle characteristics as a function of age. , 1982, Sleep.

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

[56]  G. Ratcliff,et al.  Sex differences in brain aging: a quantitative magnetic resonance imaging study. , 1998, Archives of neurology.

[57]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

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

[59]  Hans-Peter Landolt,et al.  Age-dependent changes in sleep EEG topography , 2001, Clinical Neurophysiology.

[60]  P. Achermann,et al.  Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men , 1996, Brain Research.

[61]  H. Schulz,et al.  Topographical analysis of sleep spindle activity. , 1992, Neuropsychobiology.

[62]  C. Fennema-Notestine,et al.  Effects of age on tissues and regions of the cerebrum and cerebellum , 2001, Neurobiology of Aging.

[63]  P. Achermann,et al.  Functional topography of the human nonREM sleep electroencephalogram , 2001, The European journal of neuroscience.

[64]  W R Jankel,et al.  Sleep Spindles , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[65]  T. Sejnowski,et al.  Thalamic and thalamocortical mechanisms underlying 3 Hz spike-and-wave discharges. , 1999, Progress in brain research.