The Effects of Sleep Deprivation on Brain Functioning in Older Adults

Few studies have examined the effects of total sleep deprivation (TSD) on cognitive performance and brain activation using functional MRI (fMRI) in older adults. The current study examines blood oxygen level-dependent (BOLD) activation in older adults and younger adults during the sustained attention (GO) and response inhibition (NOGO) portions of a GO-NOGO cognitive task following 36 hr of total sleep deprivation. No significant performance differences were observed between the groups on the behavioral outcome measures of total hits and false alarms. Neuroimaging results, however, revealed a significant interaction between age-group and sleep-deprivation status. Specifically, older adults showed greater BOLD activation as compared to younger adults after 36 hours total sleep deprivation in brain regions typically associated with attention and inhibitory processes. These results suggest in order for older adults to perform the GO-NOGO task effectively after sleep deprivation, they rely on compensatory recruitment of brain regions that aide in the maintenance of cognitive performance.

[1]  M. Paulus,et al.  Effects of two nights sleep deprivation and two nights recovery sleep on response inhibition , 2006, Journal of sleep research.

[2]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[3]  M. Chee,et al.  Functional Imaging of Working Memory after 24 Hr of Total Sleep Deprivation , 2004, The Journal of Neuroscience.

[4]  Gregory G. Brown,et al.  Altered brain response to verbal learning following sleep deprivation , 2000, Nature.

[5]  M. Schoonheim,et al.  Sleep benefits subsequent hippocampal functioning , 2009, Nature Neuroscience.

[6]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[7]  S. Ancoli-Israel,et al.  Preclinical cognitive decline and subsequent sleep disturbance in older women , 2007, Neurology.

[8]  Gregory G. Brown,et al.  Increased cerebral response during a divided attention task following sleep deprivation , 2001, Journal of sleep research.

[9]  S. Ancoli-Israel,et al.  Relationship between obstructive sleep apnea severity and brain activation during a sustained attention task. , 2009, Sleep.

[10]  R. Rosa,et al.  Sleep and performance in young adults and older normals and insomniacs during acute sleep loss and recovery , 1987, Biological Psychology.

[11]  S. Golaszewski,et al.  Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. , 2002, Brain : a journal of neurology.

[12]  M. J. Meloy,et al.  The neural basis of the psychomotor vigilance task. , 2005, Sleep.

[13]  Sheng He,et al.  A functional MRI study of high-level cognition. I. The game of chess. , 2003, Brain research. Cognitive brain research.

[14]  C. Czeisler,et al.  Healthy Older Adults Better Tolerate Sleep Deprivation Than Young Adults , 2009, Journal of the American Geriatrics Society.

[15]  M. Russo,et al.  EFFECTS OF SLEEP DEPRIVATION ON LATERAL VISUAL ATTENTION , 2006, The International journal of neuroscience.

[16]  B. Bioulac,et al.  Age, performance and sleep deprivation , 2004, Journal of sleep research.

[17]  M. Bonnet The effect of sleep fragmentation on sleep and performance in younger and older subjects , 1989, Neurobiology of Aging.

[18]  T. Gill,et al.  Sleep Complaints in Community‐Living Older Persons: A Multifactorial Geriatric Syndrome , 2007, Journal of the American Geriatrics Society.

[19]  C. Koch,et al.  What is the function of the claustrum? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  R. Cabeza Cognitive neuroscience of aging: contributions of functional neuroimaging. , 2001, Scandinavian journal of psychology.

[21]  M. Paulus,et al.  Functional MRI of inhibitory processing in abstinent adolescent marijuana users , 2007, Psychopharmacology.

[22]  Anthony R. McIntosh,et al.  Age-Related Differences in Neural Activity during Memory Encoding and Retrieval: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[23]  Martin P Paulus,et al.  Dissociation of inhibition from error processing using a parametric inhibitory task during functional magnetic resonance imaging , 2005, Neuroreport.

[24]  Steve Majerus,et al.  Neural Correlates of Ongoing Conscious Experience: Both Task-Unrelatedness and Stimulus-Independence Are Related to Default Network Activity , 2011, PloS one.

[25]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[26]  Jacqueline Gottlieb,et al.  Spatial and non-spatial functions of the parietal cortex , 2010, Current Opinion in Neurobiology.

[27]  M. Czisch,et al.  On the Need of Objective Vigilance Monitoring: Effects of Sleep Loss on Target Detection and Task-Negative Activity Using Combined EEG/fMRI , 2012, Front. Neur..

[28]  M. Johns,et al.  A new method for measuring daytime sleepiness: the Epworth sleepiness scale. , 1991, Sleep.

[29]  C. Frith,et al.  A Specific Role for the Thalamus in Mediating the Interaction of Attention and Arousal in Humans , 1998, The Journal of Neuroscience.

[30]  Y. D. van der Werf,et al.  Do sleep complaints contribute to age-related cognitive decline? , 2010, Progress in brain research.

[31]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[32]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[33]  J. Horne,et al.  Gender- and age-related differences in sleep determined by home-recorded sleep logs and actimetry from 400 adults. , 1995, Sleep.

[34]  Scott T. Grafton,et al.  Compensatory recruitment of neural resources during overt rehearsal of word lists in Alzheimer's disease. , 1998, Neuropsychology.

[35]  P. Polo-Kantola,et al.  Sleep deprivation: Impact on cognitive performance , 2007, Neuropsychiatric disease and treatment.

[36]  M. Walker,et al.  Neural correlates of working memory performance in primary insomnia. , 2013, Sleep.

[37]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[38]  A. Marks,et al.  The relationship between poor sleep and inhibitory functions indicated by event-related potentials , 2008, Experimental Brain Research.

[39]  C. Guilleminault,et al.  Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. , 2004, Sleep.

[40]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[41]  J. Pekar,et al.  Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent , 2008, Neuropsychologia.

[42]  Gregory G. Brown,et al.  The Effects of Total Sleep Deprivation on Cerebral Responses to Cognitive Performance , 2001, Neuropsychopharmacology.

[43]  T. Balkin,et al.  Age and individual variability in performance during sleep restriction , 2006, Journal of sleep research.

[44]  T. Balkin,et al.  Impaired decision making following 49 h of sleep deprivation , 2006, Journal of sleep research.

[45]  Sonia Ancoli-Israel,et al.  Sleep in the elderly: normal variations and common sleep disorders. , 2008, Harvard review of psychiatry.

[46]  D. Dinges,et al.  A meta-analysis of the impact of short-term sleep deprivation on cognitive variables. , 2010, Psychological bulletin.

[47]  S. Ancoli-Israel,et al.  Sleep, health, and aging. Bridging the gap between science and clinical practice. , 2004, Geriatrics.

[48]  J. Cauley,et al.  Poor sleep is associated with impaired cognitive function in older women: the study of osteoporotic fractures. , 2006, The journals of gerontology. Series A, Biological sciences and medical sciences.

[49]  P. Maruff,et al.  The Development of Sustained Attention in Children: The Effect of Age and Task Load , 2006, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[50]  E. de Luca d'Alessandro,et al.  Aging populations: the health and quality of life of the elderly. , 2011, La Clinica terapeutica.

[51]  J. Grafman,et al.  The roles of the cerebellum and basal ganglia in timing and error prediction , 2002, The European journal of neuroscience.

[52]  Lawrence Edelstein,et al.  Hypotheses relating to the function of the claustrum , 2012, Front. Integr. Neurosci..

[53]  John J. Foxe,et al.  A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. , 2004, Brain research. Cognitive brain research.

[54]  M. J. Meloy,et al.  Compensatory recruitment after sleep deprivation and the relationship with performance , 2005, Psychiatry Research: Neuroimaging.

[55]  Sonia Ancoli-Israel,et al.  Sleep and its disorders in aging populations. , 2009, Sleep medicine.

[56]  J. Marquié,et al.  Effects of working conditions and sleep of the previous day on cognitive performance. , 2008, Applied ergonomics.

[57]  M. Chee,et al.  Lapsing during Sleep Deprivation Is Associated with Distributed Changes in Brain Activation , 2008, The Journal of Neuroscience.

[58]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[59]  Mirjam Münch,et al.  Gender and age differences in psychomotor vigilance performance under differential sleep pressure conditions , 2006, Behavioural Brain Research.

[60]  Leslie G. Ungerleider,et al.  Age-related changes in cortical blood flow activation during visual processing of faces and location , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[62]  D. Dinges,et al.  Neurocognitive Consequences of Sleep Deprivation , 2005, Seminars in neurology.

[63]  Sheng He,et al.  A functional MRI study of high-level cognition , 2003 .

[64]  P. Prinz Sleep and Sleep Disorders in Older Adults , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[65]  Sonia Ancoli-Israel,et al.  Altered brain activation during response inhibition in obstructive sleep apnea , 2009, Journal of sleep research.

[66]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[67]  Gian Luca Romani,et al.  Somato-motor inhibitory processing in humans: An event-related functional MRI study , 2008, NeuroImage.

[68]  R. Bootzin,et al.  Understanding and treating insomnia. , 2011, Annual review of clinical psychology.

[69]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[70]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[71]  Gregory G. Brown,et al.  Increasing task difficulty facilitates the cerebral compensatory response to total sleep deprivation. , 2004, Sleep.