How acute total sleep loss affects the attending brain: a meta-analysis of neuroimaging studies.

STUDY OBJECTIVES Attention is a cognitive domain that can be severely affected by sleep deprivation. Previous neuroimaging studies have used different attention paradigms and reported both increased and reduced brain activation after sleep deprivation. However, due to large variability in sleep deprivation protocols, task paradigms, experimental designs, characteristics of subject populations, and imaging techniques, there is no consensus regarding the effects of sleep loss on the attending brain. The aim of this meta-analysis was to identify brain activations that are commonly altered by acute total sleep deprivation across different attention tasks. DESIGN Coordinate-based meta-analysis of neuroimaging studies of performance on attention tasks during experimental sleep deprivation. METHODS The current version of the activation likelihood estimation (ALE) approach was used for meta-analysis. The authors searched published articles and identified 11 sleep deprivation neuroimaging studies using different attention tasks with a total of 185 participants, equaling 81 foci for ALE analysis. RESULTS The meta-analysis revealed significantly reduced brain activation in multiple regions following sleep deprivation compared to rested wakefulness, including bilateral intraparietal sulcus, bilateral insula, right prefrontal cortex, medial frontal cortex, and right parahippocampal gyrus. Increased activation was found only in bilateral thalamus after sleep deprivation compared to rested wakefulness. CONCLUSION Acute total sleep deprivation decreases brain activation in the fronto-parietal attention network (prefrontal cortex and intraparietal sulcus) and in the salience network (insula and medial frontal cortex). Increased thalamic activation after sleep deprivation may reflect a complex interaction between the de-arousing effects of sleep loss and the arousing effects of task performance on thalamic activity.

[1]  Jane R. Garrison,et al.  Prediction error in reinforcement learning: A meta-analysis of neuroimaging studies , 2013, Neuroscience & Biobehavioral Reviews.

[2]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

[3]  A. Pack,et al.  Heritability of performance deficit accumulation during acute sleep deprivation in twins. , 2012, Sleep.

[4]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[5]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[6]  M. Walker,et al.  Sleep Deprivation Amplifies Reactivity of Brain Reward Networks, Biasing the Appraisal of Positive Emotional Experiences , 2011, The Journal of Neuroscience.

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

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

[9]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[10]  Vinod Venkatraman,et al.  Sleep deprivation elevates expectation of gains and attenuates response to losses following risky decisions. , 2007, Sleep.

[11]  D. Dinges,et al.  The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. , 2003, Sleep.

[12]  Carrie R. H. Innes,et al.  Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. , 2012, Sleep.

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

[14]  Kevin A. Johnson,et al.  Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation. , 2005, Sleep.

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

[16]  Niels Birbaumer,et al.  Temporo-Spatial Dynamics of Event-Related EEG Beta Activity during the Initial Contingent Negative Variation , 2010, PloS one.

[17]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[18]  A. Luria The Working Brain , 1973 .

[19]  H. Rao ASL imaging of brain function changes during sleep restriction. , 2012, Sleep.

[20]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[21]  D. Dinges,et al.  Sleep, circadian rhythms, and psychomotor vigilance. , 2005, Clinics in sports medicine.

[22]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

[24]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[25]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[26]  Brendan E. Depue,et al.  A neuroanatomical model of prefrontal inhibitory modulation of memory retrieval , 2012, Neuroscience & Biobehavioral Reviews.

[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]  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.

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

[30]  Michael W. L. Chee,et al.  Reduced visual processing capacity in sleep deprived persons , 2011, NeuroImage.

[31]  Lisa Y. M. Chuah,et al.  Sleep Deprivation Biases the Neural Mechanisms Underlying Economic Preferences , 2010, The Journal of Neuroscience.

[32]  D. Kerzel,et al.  Salient stimuli capture attention and action , 2013, Attention, Perception, & Psychophysics.

[33]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[34]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[35]  Frank Van Overwalle,et al.  Social cognition and the cerebellum: A meta-analysis of over 350 fMRI studies , 2014, NeuroImage.

[36]  Hengyi Rao,et al.  The role of human parietal cortex in attention networks. , 2003, Brain : a journal of neurology.

[37]  Stephen J. Boies,et al.  Components of attention. , 1971 .

[38]  G. Vandewalle,et al.  Light as a modulator of cognitive brain function , 2009, Trends in Cognitive Sciences.

[39]  M. Walker,et al.  The impact of sleep deprivation on food desire in the human brain , 2013, Nature Communications.

[40]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[41]  Alan C. Evans,et al.  Time-Related Changes in Neural Systems Underlying Attention and Arousal During the Performance of an Auditory Vigilance Task , 1997, Journal of Cognitive Neuroscience.

[42]  R. Croft,et al.  The effect of sleep deprivation on BOLD activity elicited by a divided attention task , 2011, Brain Imaging and Behavior.

[43]  G. Vandewalle,et al.  Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components , 2012, Journal of sleep research.

[44]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[45]  M. Buchsbaum,et al.  Frontal Lobe Metabolic Decreases with Sleep Deprivation not Totally Reversed by Recovery Sleep , 2006, Neuropsychopharmacology.

[46]  J. Coull Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology , 1998, Progress in Neurobiology.

[47]  Michael W. L. Chee,et al.  Sleep deprivation and its effects on object-selective attention , 2010, NeuroImage.

[48]  J. Mattingley Attention, Consciousness, and the Damaged Brain: Insights From Parietal Neglect and Extinction , 1999 .

[49]  Judi E. See,et al.  Brain systems of vigilance. , 1998 .

[50]  Michael W. L. Chee,et al.  Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: Correlations of fronto-parietal activation with performance , 2006, NeuroImage.

[51]  Joshua W. Brown,et al.  A meta-analysis of executive components of working memory. , 2013, Cerebral cortex.

[52]  M. Buchsbaum,et al.  The effect of sleep deprivation on cerebral glucose metabolic rate in normal humans assessed with positron emission tomography. , 1991, Sleep.

[53]  M. Chee,et al.  Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task. , 2007, Sleep.

[54]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

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

[56]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[57]  John A. Detre,et al.  Imaging brain fatigue from sustained mental workload: An ASL perfusion study of the time-on-task effect , 2010, NeuroImage.

[58]  Alexandra Sebastian,et al.  A coordinate-based ALE functional MRI meta-analysis of brain activation during verbal fluency tasks in healthy control subjects , 2014, BMC Neuroscience.

[59]  Y. Tsai,et al.  Mapping gray matter reductions in obstructive sleep apnea: an activation likelihood estimation meta-analysis. , 2014, Sleep.

[60]  N. Schiff Central Thalamic Contributions to Arousal Regulation and Neurological Disorders of Consciousness , 2008, Annals of the New York Academy of Sciences.

[61]  D. Dinges,et al.  Sleep Deprivation and Vigilant Attention , 2008, Annals of the New York Academy of Sciences.

[62]  Maria L. Thomas,et al.  Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity , 2000, Journal of sleep research.

[63]  Michael W. L. Chee,et al.  Effects of sleep deprivation on cortical activation during directed attention in the absence and presence of visual stimuli , 2011, NeuroImage.

[64]  Adam R. Walczak,et al.  At the heart of the ventral attention system: The right anterior insula , 2009, Human brain mapping.

[65]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[66]  M. Chee,et al.  Sleep Deprivation Impairs Object-Selective Attention: A View from the Ventral Visual Cortex , 2010, PloS one.

[67]  Caroline G. Soule Egg-Laying of Limenitis Disippus , 1888 .

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

[69]  D. Dinges,et al.  Neurocognitive consequences of sleep deprivation. , 2005, Seminars in neurology.

[70]  Jonathan D. Cohen,et al.  Anterior cingulate and prefrontal cortex: who's in control? , 2000, Nature Neuroscience.

[71]  Michael W. L. Chee,et al.  Lapsing when sleep deprived: Neural activation characteristics of resistant and vulnerable individuals , 2010, NeuroImage.

[72]  Michael W. L. Chee,et al.  Functional imaging correlates of impaired distractor suppression following sleep deprivation , 2012, NeuroImage.

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

[74]  D. Dinges,et al.  Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. , 2004, Sleep.

[75]  Michael W. L. Chee,et al.  Dissociation of cortical regions modulated by both working memory load and sleep deprivation and by sleep deprivation alone , 2005, NeuroImage.

[76]  D. Dinges,et al.  Sleep deprivation and neurobehavioral dynamics , 2013, Current Opinion in Neurobiology.

[77]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

[78]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[79]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[80]  J. Mcdowd,et al.  An Overview of Attention: Behavior and Brain , 2007, Journal of neurologic physical therapy : JNPT.

[81]  M. Lindquist,et al.  Meta-analysis of functional neuroimaging data: current and future directions. , 2007, Social cognitive and affective neuroscience.

[82]  I. Radermacher,et al.  Functional anatomy of intrinsic alertness: evidencefor a fronto-parietal-thalamic-brainstem network in theright hemisphere , 1999, Neuropsychologia.

[83]  R. Dolan,et al.  The Neural Correlates of the Noradrenergic Modulation of Human Attention, Arousal and Learning , 1997, The European journal of neuroscience.

[84]  Aleksandra Shkurko Is social categorization based on relational ingroup/outgroup opposition? A meta-analysis. , 2013, Social cognitive and affective neuroscience.

[85]  S. Eickhoff,et al.  Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. , 2013, Psychological bulletin.

[86]  Jejo D. Koola,et al.  Decreased cortical response to verbal working memory following sleep deprivation. , 2005, Sleep.

[87]  K. Davis,et al.  Two systems of resting state connectivity between the insula and cingulate cortex , 2009, Human brain mapping.

[88]  E. Zarahn,et al.  An event-related fMRI study of the neurobehavioral impact of sleep deprivation on performance of a delayed-match-to-sample task. , 2004, Brain research. Cognitive brain research.

[89]  Michael P Milham,et al.  The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[90]  Michael W. L. Chee,et al.  Time-on-task and sleep deprivation effects are evidenced in overlapping brain areas , 2013, NeuroImage.

[91]  Todd B. Parrish,et al.  Sleep deprivation alters functioning within the neural network underlying the covert orienting of attention , 2008, Brain Research.

[92]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[93]  Kaustubh Supekar,et al.  Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. , 2010, Cerebral cortex.

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

[95]  N. Volkow,et al.  Impairment of attentional networks after 1 night of sleep deprivation. , 2009, Cerebral cortex.

[96]  H. Diener,et al.  On the neural basis of focused and divided attention. , 2005, Brain research. Cognitive brain research.