Brain Activity in Sleep Compared to Wakefulness: A Meta-Analysis

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DOI: 10.4236/jbbs.2012.22028    3,538 Downloads   7,569 Views   Citations


Objective: Neuroimaging studies using a variety of techniques have been conducted in sleep to explore the changes in brain activity during the different sleep stages. The current study employed a quantitative meta-analytic technique in an attempt to integrate the findings from such studies. Methods: Using an updated version of the Activation Likelihood Estimation (ALE) method, individual meta-analyses were carried out on: 1) studies contrasting REM sleep and wakefulness, and 2) studies contrasting NREM sleep and wakefulness. Results: Based on the results of the current meta-analyses, a number of cortical and subcortical brain regions appear to be involved in sleep and sleep processes, with both decreases and increases noted across NREM and REM sleep. Specifically, areas of decreased activity comprised thalamic structures (pulvinar, dorsomedial thalamus) and frontal regions (inferior, superior, and middle frontal gyrus). Furthermore, increased and decreased activity was noted in the anterior cingulate during sleep. Conclusions: Despite limited overlap across these sleep stages among regions identified, consistent decreases were revealed in NREM sleep (thalamus) and REM sleep (frontal cortex) when compared to wakefulness. Such findings suggest that these regions may ultimately play a key role in the loss of consciousness characteristic of sleep. Further research is needed to determine if and how such activity may be related to dreaming.

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A. Jakobson, A. Laird, J. Maller, R. Conduit and P. Fitzgerald, "Brain Activity in Sleep Compared to Wakefulness: A Meta-Analysis," Journal of Behavioral and Brain Science, Vol. 2 No. 2, 2012, pp. 249-257. doi: 10.4236/jbbs.2012.22028.


[1] E. Aserinsky and N. Kleitman, “Regularly Occurring Periods of Eye Motility and Concomitant Phenomena during Sleep,” Science, Vol. 118, No. 3062, 1953, pp. 273-274. doi:10.1126/science.118.3062.273
[2] J. A. Hobson, E. F. Pace-Schott and R. Stickgold, “Dreaming and the Brain: Toward a Cognitive Neuroscience of Conscious States,” Behavioral and Brain Sciences, Vol. 23, No. 6, 2000, pp. 793-842. doi:10.1017/S0140525X00003976
[3] M. Solms, “Dreaming and REM Sleep Are Controlled by Different Brain Mechanisms,” Behavioral and Brain Sciences, Vol. 23, No. 6, 2000, pp. 843-850. doi:10.1017/S0140525X00003988
[4] P. T. Fox, L. M. Parsons and J. L. Lancaster, “Beyond the Single Study: Function/Location Metanalysis in Cognitive Neuroimaging,” Current Opinion in Neurobiology, Vol. 8, No. 2, 1998, pp. 178-187. doi:10.1016/S0959-4388(98)80138-4
[5] P. E. Turkeltaub, G. F. Eden, K. M. Jones and T. A. Zeffiro, “Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation,” Neuroimage, Vol. 16, No. 3, 2002, pp. 765-780. doi:10.1006/nimg.2002.1131
[6] S. B. Eickhoff, A. R. Laird, C. Grefkes, L. E. Wang, K. Zilles and P. T. Fox, “Coordinate-Based ALE Meta-Analysis of Neuroimaging Data: A Random-Effects Approach Based on Empirical Estimates of Spatial Uncertainty,” Human Brain Mapping, Vol. 30, No. 9, 2009, pp. 2907-2926. doi:10.1002/hbm.20718
[7] N. Hofle, T. Paus, D. Reutens, P. Fiset, J. Gotman, A. C. Evans and B. E. Jones, “Regional Cerebral Blood Flow Changes as a Function of Delta and Spindle Activity during Slow Wave Sleep in Humans,” Journal of Neuroscience, Vol. 17, No. 12, 1997, pp. 4800-4808.
[8] T. W. Kjaer, I. Law, G. Wiltschi?tz, O. B. Paulson and P. L. Madsen, “Regional Cerebral Blood Flow during Light Sleep—A H(2)(15)O-PET Study,” Journal of Sleep Research, Vol. 11, No. 3, 2002, pp. 201-207. doi:10.1046/j.1365-2869.2002.00303.x
[9] J. L. Lancaster, D. Tordesillas-Gutiérrez, M. Martinez, F. Salinas, A. Evans, K. Zilles, J. C. Mazziotta and P. T. Fox, “Bias between MNI and Talairach Coordinates Analyzed Using ICBM-152 Brain Template,” Human Brain Mapping, Vol. 28, No. 11, 2007, pp. 1194-1205. doi:10.1002/hbm.20345
[10] P. T. Fox and J. L. Lancaster, “Mapping Context and Content: The BrainMap Model,” Nature Reviews Neuroscience, Vol. 3, No. 4, 2002, pp. 319-321. doi:10.1038/nrn789
[11] A. R. Laird, J. L. Lancaster and P. T. Fox, “BrainMap: The Social Evolution of a Functional Neuroimaging Database,” Neuroinformatics, Vol. 3, No. 1, 2005, pp. 65-78. doi:10.1385/NI:3:1:065
[12] A. R. Laird, P. M. Fox, C. J. Price, D. C. Glahn, A. M. Uecker, J. L. Lancaster, P. E. Turkeltaub, P. Kochunov and P. T. Fox, “ALE Meta-Analysis: Controlling the False Discovery Rate and Performing Statistical Contrasts,” Human Brain Mapping, Vol. 25, No. 1, 2005, pp. 155-164. doi:10.1002/hbm.20136
[13] J. L. Lancaster, M. G. Woldorff, L. M. Parsons, M. Liotti, C. S. Freitas, L. Rainey, P. V. Kochunov, D. Nickerson, S. A. Mikiten and P. T. Fox, “Automated Talairach Atlas Labels for Functional Brain Mapping,” Human Brain Mapping, Vol. 10, No. 3, 2000, pp. 120-131. doi:10.1002/1097-0193(200007)10:3<120::AID-HBM30>3.0.CO;2-8
[14] P. Kochunov, J. Lancaster, P. Thompson, A. W. Toga, P. Brewer, J. Hardies and P. Fox, “An Optimized Individual Target Brain in the Talairach Coordinate System,” Neuroimage, Vol. 17, No. 2, 2002, pp. 922-927. doi:10.1006/nimg.2002.1084
[15] M. Schabus, T. T. Dang-Vu, G. Albouy, E. Balteau, M. Boly, J. Carrier, A. Darsaud, C. Degueldre, M. Desseilles, S. Gais, C. Phillips, G. Rauchs, C. Schnakers, V. Sterpenich, G. Vandewalle, A. Luxen and P. Maquet, “Hemodynamic Cerebral Correlates of Sleep Spindles during Human Non-Rapid Eye Movement Sleep,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 32, 2007, pp. 13164-13169. doi:10.1073/pnas.0703084104
[16] M. Steriade, “The Corticothalamic System in Sleep,” Frontiers in Bioscience, Vol. 8, 2003, pp. 878-899. doi:10.2741/1043
[17] P. Cortelli, D. Perani, P. Montagna, R. Gallassi, P. Tinuper, F. Provini, P. Avoni, F. Ferrillo, D. Anchisi, R. M. Moresco, F. Fazio, P. Parchi, A. Baruzzi, E. Lugaresi and P. Gambetti, “Pre-Symptomatic Diagnosis in Fatal Familial Insomnia: Serial Neurophysiological and [18F] FDG PET Studies,” Brain, Vol. 129, No. 3, 2006, pp. 668-675. doi:10.1093/brain/awl003
[18] V. Manetto, R. Medori, P. Cortelli, P. Montagna, P. Tinuper, A. Baruzzi, G. Rancurel, J. J. Hauw, J. J. van Derhaeghen, P. Mailleux, O. Bugiani, F. Tagliavini, C. Bouras, N. Rizzuto, E. Lugaresi and P. Gambetti, “Fatal Familial Insomnia: Clinical and Pathologic Study of Five New Cases,” Neurology, Vol. 42, No. 2, 1992, pp. 312- 319.
[19] P. Montagna, F. Provini, G. Plazzi, R. Vetrugno, R. Gallassi, G. Pierangeli, M. Ragno, P. Cortelli and D. Perani, “Bilateral Paramedian Thalamic Syndrome: Abnormal Circadian Wake-Sleep and Autonomic Functions,” Journal of Neurology, Neurosurgery, and Psychiatry, Vol. 73, No. 6, 2002, pp. 772-774. doi:10.1136/jnnp.73.6.772
[20] J. Nolte, “The Human Brain: An Introduction to Its Functional Anatomy,” 6th Edition, Mosby, Edinburgh, 2008.
[21] J. H. Martin, “Neuroanatomy: Text and Atlas,” 3rd Edition, McGraw-Hill, New York, 2003.
[22] Y. D. Van der Werf, J. Jolles, M. P. Witter and H. B. Uylings, “Contributions of Thalamic Nuclei to Declarative Memory Functioning,” Cortex, Vol. 39, No. 4-5, 2003, pp. 1047-1062. doi:10.1016/S0010-9452(08)70877-3
[23] A. R. Braun, T. J. Balkin, N. J. Wesensten, R. E. Carson, M. Varga, P. Baldwin, S. Selbie, G. Belenky and P. Herscovitch, “Regional Cerebral Blood Flow throughout the Sleep-Wake Cycle: An H215O PET Study,” Brain, Vol. 120, No. 7, 1997, pp. 1173-1197. doi:10.1093/brain/120.7.1173
[24] C. M. Portas, G. Rees, A. M. Howseman, O. Josephs, R. Turner and C. D. Frith, “A Specific Role for the Thalamus in Mediating the Interaction of Attention and Arousal in Humans,” Journal of Neuroscience, Vol. 18, No. 21, 1999, pp. 8879-8989.
[25] M. Mancia and G. Marini, “Thalamic Mechanisms in Sleep Control,” In: O. Hayaishi and S. Inoue, Eds., Sleep and Sleep Disorders: From Molecule to Behavior, Academic Press, London, 1997, pp. 377-393.
[26] P. Maquet, D. Dive, E. Salmon, B. Sadzot, G. Franco, R. Poirrier and G. Franck, “Cerebral Glucose Utilization During Stage 2 Sleep in Man,” Brain Research, Vol. 571, No. 1, 1992, pp. 149-153. doi:10.1016/0006-8993(92)90522-B
[27] P. D. Zelazo and U. Muller, “Executive Function in Typical and Atypical Development,” In: U. Goswam, Ed., Blackwell Handbook of Child Cognitive Development, Blackwell Publishing, Oxford, 2002, pp. 445-469. doi:10.1002/9780470996652.ch20
[28] M. L. Kringelbach, “The Human Orbitofrontal Cortex: Linking Reward to Hedonic Experience,” Nature Reviews Neuroscience, Vol. 6, No. 9, 2005, pp. 691-702. doi:10.1038/nrn1747
[29] A. Baddely, “Recent Developments in Working Memory,” Current Opinion in Neurobiology, Vol. 8, No. 2, 1998, pp. 234-238. doi:10.1016/S0959-4388(98)80145-1
[30] A. Bechara, A. R. Damasio, H. Damasio and S. W. Anderson, “Insensitivity to Future Consequences Following Damage to Human Prefrontal Cortex,” Cognition, Vol. 50, No. 1-3, 1994, pp. 7-15. doi:10.1016/0010-0277(94)90018-3
[31] J. B. Brewer, Z. Zhao, J. E. Desmond, G. H. Glover and J. D. Gabrieli, “Making Memories: Brain Activity that Predicts How Well Visual Experience Will Be Remembered,” Science, Vol. 281, No. 5380, 1998, pp. 1185-1187. doi:10.1126/science.281.5380.1185
[32] P. Maquet and G. Franck, “REM Sleep and Amygdale,” Molecular Psychiatry, Vol. 2, No. 3, 1997, pp. 195-196. doi:10.1038/
[33] R. Stickgold, E. F. Pace-Schott and J. A. Hobson, “Subjective Estimates of Dream Duration and Dream Recall Process,” Sleep Research, Vol. 26, 1997, p. 279.
[34] J. A. Hobson, R. Stickgold and E. F. Pace-Schott, “The Neuropsychology of REM Sleep Dreaming,” Neuroreport, Vol. 9, No. 3, 1998, pp. 1-14. doi:10.1097/00001756-199802160-00033
[35] J. A. Hobson, S. A. Hoffman, R. Helfand and D. Kostner, “Dream Bizarreness and the Activation-Synthesis Hypothesis,” Human Neurobiology, Vol. 6, No. 3, 1987, pp. 157-164.
[36] A. Pissiota, O. Frans, A. Michelgard, L. Appel, B. Langstrom, M. A. Flaten and M. Fredrikson, “Amygdala and Anterior Cingulate Cortex Activation during Affective Startle Modulation: A Pet Study of Fear,” European Journal of Neuroscience, Vol. 18, No. 5, 2003, pp. 1325-1331. doi:10.1046/j.1460-9568.2003.02855.x
[37] M. Corbetta, F. M. Miezin, S. Dobmeyer, G. L. Shulman and S. E. Petersen, “Selective and Divided Attention during Visual Discriminations of Shape, Color and Speed: Functional Anatomy by Positron Emission Tomography,” Journal of Neuroscience, Vol. 11, No. 8, 1991, pp. 2383-2402.
[38] J. D. Cohen, M. Botvinick and C. S. Carter, “Anterior Cingulate and Prefrontal Cortex: Who’s in Control?” Na- ture Neuroscience, Vol. 3, No. 5, 2000, pp. 421-423.
[39] S. Dehaene, M. I. Posner and D. M. Tucker, “Localization of a Neural System for Error Detection and Compensation,” Psychological Science, Vol. 5, 1994, pp. 303-305. doi:10.1111/j.1467-9280.1994.tb00630.x
[40] B. A. Vogt, P. R. Hof and L. J. Vogt, “Cingulate Gyrus,” In: G. Paxinos and J. K. Mai, Eds., The Human Nervous System, 2nd Edition, Academic Press, San Diego, 2004, pp. 915-949. doi:10.1016/B978-012547626-3/50025-9
[41] M. Murphy, B. A. Riedner, R. Huber, M. Massimini, F. Ferrarelli and G. Tononi, “Source Modeling Sleep Slow Waves,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 5, 2009, pp. 1608-1613. doi:10.1073/pnas.0807933106
[42] P. Maquet, J. M. Peters, J. Aerts, G. Delfiore, C. Deguel- dre, A. Luxen and G. Franck, “Functional Neuroanatomy of Human Rapid-Eye-Movement Sleep and Dreaming,” Nature, Vol. 383, No. 6596, 1996, pp. 163-166. doi:10.1038/383163a0
[43] P. Maquet, C. Degueldre, G. Delfiore, J. Aerts, J. M. Peters, A. Luxen and G. Franck, “Functional Neuroanatomy of Human Slow Wave Sleep,” Journal of Neuroscience, Vol. 17, No. 8, 1997, pp. 2807-2812.
[44] A. R. Braun, T. J. Balkin, N. J. Wesensten, F. Gwadry, R. E. Carson and M. Varga, “Dissociated Pattern of Activity in Visual Cortices and Their Projections during Human Rapid Eye Movement Sleep,” Science, Vol. 279, No. 5347, 1998, pp. 91-95. doi:10.1126/science.279.5347.91

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