Sleep-wake differences in relative regional cerebral metabolic rate for glucose among patients with insomnia compared with good sleepers

Sleep

Volumn 39, Issue 10, 2016, Pages 1779-1794

  Kay, Daniel B ^a   Karim, Helmet T ^b   Soehner, Adriane M ^a   Hasler, Brant P ^a   Wilckens, Kristine A ^a   James, Jeffrey A ^c   Aizenstein, Howard J ^a   Price, Julie C ^c   Rosario, Bedda L ^e   Kupfer, David J ^a   Germain, Anne ^a   Hall, Martica H ^a   Franzen, Peter L ^a   Nofzinger, Eric A ^a,d   Buysse, Daniel J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b University of Pittsburgh   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d Cerêve Inc   (United States)

^e UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

FDG; Insomnia; Neuroimaging; PET

Indexed keywords

FLUORODEOXYGLUCOSE F 18; GLUCOSE;

ADULT; AMYGDALA; ANTERIOR CINGULATE; ARTICLE; BRAIN METABOLISM; BRAIN REGION; CEREBELLUM; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; FUSIFORM GYRUS; GLUCOSE METABOLISM; HUMAN; INFERIOR PARIETAL LOBULE; INSULA; LINGUAL GYRUS; MALE; MEDIAL FRONTAL CORTEX; METABOLIC RATE; MIDDLE FRONTAL GYRUS; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; NONREM SLEEP; OCCIPITAL CORTEX; OCCIPITAL GYRUS; POSITRON EMISSION TOMOGRAPHY; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PRECUNEUS; PREMOTOR CORTEX; PRIMARY INSOMNIA; PRIORITY JOURNAL; REGIONAL CEREBRAL METABOLIC RATE FOR GLUCOSE; RIGHT HIPPOCAMPUS; SLEEP QUALITY; SLEEP TIME; SLEEP WAKING CYCLE; SUPERIOR PARIETAL LOBULE; SUPRAMARGINAL GYRUS; TEMPORAL CORTEX; THALAMUS; WAKEFULNESS; BRAIN; DIAGNOSTIC IMAGING; ENERGY METABOLISM; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; SLEEP; SLEEP INITIATION AND MAINTENANCE DISORDERS; YOUNG ADULT;

ADULT; BRAIN; ENERGY METABOLISM; FEMALE; FLUORODEOXYGLUCOSE F18; GLUCOSE; HUMANS; MALE; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; SLEEP; SLEEP INITIATION AND MAINTENANCE DISORDERS; WAKEFULNESS; YOUNG ADULT;

EID: 84992364866     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.6154     Document Type: Article

References (98)

1. American Academy of Sleep Medicine. International Classification of Sleep Disorders, 3rd ed. Westchester, IL: American Academy of Sleep Medicine, 2014.
2. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Arlington, VA: American Psychiatric Association, 2013.
3. Chung KF, Yeung WF, Ho FY, Yung KP, Yu YM, Kwok CW. Crosscultural and comparative epidemiology of insomnia: the Diagnostic and Statistical Manual (DSM), International Classification of Diseases (ICD) and International Classification of Sleep Disorders (ICSD). Sleep Med 2015; 16:477-82.
4. Léger D, Bayon V. Societal costs of insomnia. Sleep Med Rev 2010; 14:379-89.
5. Parthasarathy S, Vasquez MM, Halonen M, et al. Persistent insomnia is associated with mortality risk. Am J Med 2015; 128:268-75.
6. Fortier-Brochu E, Beaulieu-Bonneau S, Ivers H, Morin CM. Insomnia and daytime cognitive performance: a meta-analysis. Sleep Med Rev 2012; 16:83-94.
7. Haimov I, Shatil E. Cognitive training improves sleep quality and cognitive function among older adults with insomnia. PLoS One 2013; 8:e61390.
8. Vincent NK, Walker JR. Perfectionism and chronic insomnia. J Psychosom Res 2000; 49:349-54.
9. Baglioni C, Battagliese G, Feige B, et al. Insomnia as a predictor of depression: a meta-analytic evaluation of longitudinal epidemiological studies. J Affect Disord 2011; 135:10-9.
10. Schmidt RE, Harvey AG, Van der Linden M. Cognitive and affective control in insomnia. Front Psychol 2011; 2:349.
11. Andrews-Hanna JR, Saxe R, Yarkoni T. Contributions of episodic retrieval and mentalizing to autobiographical thought: evidence from functional neuroimaging, resting-state connectivity, and fMRI metaanalyses. Neuroimage 2014; 91:324-35.
12. Wager TD, Smith EE. Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 2003; 3:255-74.
13. Unterrainer JM, Rahm B, Kaller CP, et al. When planning fails: individual differences and error-related brain activity in problem solving. Cereb Cortex 2004; 14:1390-7.
14. DeLeon J, Gottesman RF, Kleinman JT, et al. Neural regions essential for distinct cognitive processes underlying picture naming. Brain 2007; 130:1408-22.
15. Brühl AB, Rufer M, Kaffenberger T, Baur V, Herwig U. Neural circuits associated with positive and negative self-appraisal. Neuroscience 2014; 265:48-59.
16. Longe O, Maratos FA, Gilbert P, et al. Having a word with yourself: neural correlates of self-criticism and self-reassurance. Neuroimage 2010; 49:1849-56.
17. Sundermann B, Olde Lutke BM, Pfleiderer B. Toward literature-based feature selection for diagnostic classification: a meta-analysis of resting-state fMRI in depression. Front Hum Neurosci 2014; 8:692.
18. Groenewold NA, Opmeer EM, de J P, Aleman A, Costafreda SG. Emotional valence modulates brain functional abnormalities in depression: evidence from a meta-analysis of fMRI studies. Neurosci Biobehav Rev 2013; 37:152-63.
19. Braun AR, Balkin TJ, Wesenten NJ, et al. Regional cerebral blood flow throughout the sleep-wake cycle. An H215O PET study. Brain 1997; 120:1173-97.
20. Hofe N, Paus T, Reutens D, et al. Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J Neurosci 1997; 17:4800-8.
21. Andersson JL, Onoe H, Hetta J, et al. Brain networks affected by synchronized sleep visualized by positron emission tomography. J Cereb Blood Flow Metab 1998; 18:701-15.
22. Kajimura N, Uchiyama M, Takayama Y, et al. Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J Neurosci 1999; 19:10065-73.
23. Finelli LA, Landolt HP, Buck A, et al. Functional neuroanatomy of human sleep states after zolpidem and placebo: a H215O-PET study. J Sleep Res 2000; 9:161-73.
24. Dang-Vu TT, Desseilles M, Laureys S, et al. Cerebral correlates of delta waves during non-REM sleep revisited. Neuroimage 2005; 28:14-21.
25. Hiroki M, Uema T, Kajimura N, et al. Cerebral white matter blood flow is constant during human non-rapid eye movement sleep: a positron emission tomographic study. J Appl Physiol 2005; 98:1846-54.
26. Maquet P, Dive D, Salmon E, et al. Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-D-glucose method. Brain Res 1990; 513:136-43.
27. Maquet P, Dive D, Salmon E, et al. Cerebral glucose utilization during stage 2 sleep in man. Brain Res 1992; 571:149-53.
28. Buchsbaum MS, Hazlett EA, Wu J, Bunney WE, Jr. Positron emission tomography with deoxyglucose-F18 imaging of sleep. Neuropsychopharmacology 2001; 25:S50-6.
29. Nofzinger EA, Buysse DJ, Miewald JM, et al. Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain 2002; 125:1105-15.
30. Maquet P, Degueldre C, Delfore G, et al. Functional neuroanatomy of human slow wave sleep. J Neurosci 1997; 17:2807-12.
31. Cano G, Mochizuki T, Saper CB. Neural circuitry of stress-induced insomnia in rats. J Neurosci 2008; 28:10167-84.
32. Buysse DJ, Germain A, Hall M, Monk TH, Nofzinger EA. A neurobiological model of insomnia. Drug Discov Today Dis Models 2011; 8:129-37.
33. Nofzinger EA, Buysse DJ, Germain A, Price JC, Miewald JM, Kupfer DJ. Functional neuroimaging evidence for hyperarousal in insomnia. Am J Psychiatry 2004; 161:2126-9.
34. Riemann D, Voderholzer U, Spiegelhalder K, et al. Chronic insomnia and MRI-measured hippocampal volumes: a pilot study. Sleep 2007; 30:955-8.
35. Altena E, Vrenken H, Van Der Werf YD, van den Heuvel OA, Van Someren EJ. Reduced orbitofrontal and parietal gray matter in chronic insomnia: a voxel-based morphometric study. Biol Psychiatry 2010; 67:182-5.
36. Winkelman JW, Benson KL, Buxton OM, et al. Lack of hippocampal volume differences in primary insomnia and good sleeper controls: an MRI volumetric study at 3 Tesla. Sleep Med 2010; 11:576-82.
37. Winkelman J W, Plante DT, Schoerning L, et al. Increased rostral anterior cingulate cortex volume in chronic primary insomnia. Sleep 2013; 36:991-8.
38. Noh HJ, Joo EY, Kim ST, et al. The relationship between hippocampal volume and cognition in patients with chronic primary insomnia. J Clin Neurol 2012; 8:130-8.
39. Joo EY, Noh HJ, Kim JS, et al. Brain gray matter deficits in patients with chronic primary insomnia. Sleep 2013; 36:999-1007.
40. Joo EY, Kim H, Suh S, Hong SB. Hippocampal substructural vulnerability to sleep disturbance and cognitive impairment in patients with chronic primary insomnia: magnetic resonance imaging morphometry. Sleep 2014; 37:1189-98.
41. Spiegelhalder K, Regen W, Baglioni C, et al. Insomnia does not appear to be associated with substantial structural brain changes. Sleep 2013; 36:731-7.
42. Suh S, Kim H, Dang-Vu TT, Joo E, Shin C. Cortical thinning and altered cortico-cortical structural covariance of the default mode network in patients with persistent insomnia symptoms. Sleep 2016; 39:161-71.
43. Corsi-Cabrera M, Figueredo-Rodríguez P, del Río-Portilla Y, Sánchez-Romero J, Galán L, Bosch-Bayard J. Enhanced frontoparietal synchronized activation during the wake-sleep transition in patients with primary insomnia. Sleep 2012; 35:501-11.
44. Smith MT, Perlis ML, Chengazi VU, et al. Neuroimaging of NREM sleep in primary insomnia: a Tc-99-HMPAO single photon emission computed tomography study. Sleep 2002; 25:325-35.
45. Huang Z, Liang P, Jia X, et al. Abnormal amygdala connectivity in patients with primary insomnia: evidence from resting state fMRI. Eur J Radiol 2012; 81:1288-95.
46. Chen MC, Chang C, Glover GH, Gotlib IH. Increased insula coactivation with salience networks in insomnia. Biol Psychol 2014; 97:1-8.
47. Dai XJ, Peng DC, Gong HH, et al. Altered intrinsic regional brain spontaneous activity and subjective sleep quality in patients with chronic primary insomnia: a resting-state fMRI study. Neuropsychiatr Dis Treat 2014; 10:2163-75.
48. Li Y, Wang E, Zhang H, et al. Functional connectivity changes between parietal and prefrontal cortices in primary insomnia patients: evidence from resting-state fMRI. Eur J Med Res 2014; 19:32.
49. Nie X, Shao Y, Liu SY, et al. Functional connectivity of paired default mode network subregions in primary insomnia. Neuropsychiatr Dis Treat 2015; 11:3085-93.
50. American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 4th ed., Text Revision. Arlington, VA: American Psychiatric Association, 2000.
51. Nofzinger EA, Mintun MA, Price J, et al. A method for the assessment of the functional neuroanatomy of human sleep using FDG PET. Brain Res Protoc 1998; 2:191-8.
52. First M, Spitzer RL, Gibbon M, Williams JBW Structured Clinical Interview for DSM-IV Axis I Disorders-Patient Edition (SCID-I/P). Version 2.0. New York, NY: New York State Psychiatric Institute, 1995.
53. Beck AT, Epstein N, Brown G, Steer RA. An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 1988; 56:893-7.
54. Spielberger CD, Gorsuch RL, Luschene RE. Manual for the StateTrait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press, 1970.
55. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961; 4:561-71.
56. Rush AJ, Giles DE, Schlesser MA, Fulton CL, Weissenburger J, Burns C. The Inventory for Depressive Symptomatology (IDS): preliminary findings. Psychiatry Res 1986; 18:65-87.
57. Rush AJ, Gullion CM, Basco MR, Jarrett RB, Trivedi MH. The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychol Med 1996; 26:477-86.
58. McNair DM, Lorr M, Droppleman LF. Manual for the Profle of Mood States. San Diego, CA: Educational and Industrial Testing Service, 1971.
59. Rush AJ, Trivedi MH, Ibrahim HM, et al. The 16-Item Quick Inventory of Depressive Symptomatology (QIDS), clinician rating (QIDS-C), and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression. Biol Psychiatry 2003; 54:573-83.
60. Beck A, Steer R, Garbin M. Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clin Psychol Rev 1988; 8:77-100.
61. Julian LJ Measures of anxiety: State-Trait Anxiety Inventory (STAI), Beck Anxiety Inventory (BAI), and Hospital Anxiety and Depression Scale-Anxiety (HADS-A). Arthritis Care Res 2011; 63 Suppl 11:S467-72.
62. Facco E, Stellini E, Bacci C, et al. Validation of Visual Analogue Scale for Anxiety (VAS-A) in preanesthesia evaluation. Minerva Anestesiol 2013; 79:1389-95.
63. Grififth NM, Szaflarski JP, Szaflarski M, et al. Measuring depressive symptoms among treatment-resistant seizure disorder patients: POMS depression scale as an alternative to the BDI-II. Epilepsy Behav 2005; 7:266-72.
64. Buysse DJ, Reynolds CF III, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 1989; 28:193-213.
65. Backhaus J, Junghanns K, Broocks A, Riemann D, Hohagen F. Testretest reliability and validity of the Pittsburgh Sleep Quality Index in primary insomnia. J Psychosom Res 2002; 53:737-40.
66. Buysse DJ, Reynolds CF III, Monk TH, Hoch CC, Yeager AL, Kupfer DJ. Quantification of subjective sleep quality in healthy elderly men and women using the Pittsburgh Sleep Quality Index (PSQI). Sleep 1991; 14:331-8.
67. Monk TH, Reynolds CF, Kupfer DJ, et al. The Pittsburgh Sleep Diary. J Sleep Res 1994; 3:111-20.
68. Doman J, Detka C, Hoffman T, et al. Automating the sleep laboratory: implementation and validation of digital recording and analysis. Int J Biomed Comput 1995; 38:277-90.
69. Newell J, Mairesse O, Verbanck P, Neu D. Is a one-night stay in the lab really enough to conclude? First-night effect and night-to-night variability in polysomnographic recordings among different clinical population samples. Psychiatry Res 2012; 200:795-801.
70. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Washington, DC: US Government Printing Office, 1968.
71. Reivich M, Kuhl D, Wolf A, et al. The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circ Res 1979; 44:127-37.
72. Nofzinger EA, Price JC, Meltzer CC, et al. Towards a neurobiology of dysfunctional arousal in depression: the relationship between beta EEG power and regional cerebral glucose metabolism during NREM sleep. Psychiatry Res 2000; 98:71-91.
73. Ashburner J, Friston KJ. Unified segmentation. Neuroimage 2005; 26:839-51.
74. Woods R P, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC. Automated image registration: I. General methods and intrasubject, intramodality validation. J Comput Assist Tomogr 1998; 22:139-52.
75. Hunter GJ, Hamberg LM, Alpert NM, Choi NC, Fischman AJ. Simplified measurement of deoxyglucose utilization rate. J Nucl Med 1996; 37:950-5.
76. Gläscher J, Gitelman D. Contrast weights in flexible factorial design with multiple groups of subjects. Accessed June 19, 2016. Available from: http://www.sbirc.ed.ac.uk/cyril/download/Contrast-Weighting-Glascher-Gitelman-2008.pdf.
77. Xia MR, Wang JH, He Y. BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 2013; 8:e68910.
78. Riemann D, Spiegelhalder K, Feige B, et al. The hyperarousal model of insomnia: a review of the concept and its evidence. Sleep Med Rev 2010; 14:19-31.
79. Kattler H, Dijk DJ, Borbély AA. Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J Sleep Res 1994; 3:159-64.
80. Smith EE, Jonides J, Marshuetz C, Koeppe RA. Components of verbal working memory: evidence from neuroimaging. Proc Natl Acad Sci USA 1998; 95:876-82.
81. Kapur S, Craik FI, Tulving E, Wilson AA, Houle S, Brown GM. Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proc Natl Acad Sci USA 1994; 91:2008-11.
82. Kircher TT, Senior C, Phillips ML, et al. Towards a functional neuroanatomy of self processing: effects of faces and words. Cogn Brain Res 2000; 10:133-44.
83. Fossati P, Hevenor SJ, Lepage M, et al. Distributed self in episodic memory: neural correlates of successful retrieval of self-encoded positive and negative personality traits. Neuroimage 2004; 22:1596-604.
84. Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008; 1124:1-38.
85. Zhang S, Li CS. Functional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 2012; 59:3548-62.
86. Bench CJ, Friston KJ, Brown RG, Frackowiak RS, Dolan RJ. Regional cerebral blood flow in depression measured by positron emission tomography: the relationship with clinical dimensions. Psychol Med 1993; 23:579-90.
87. Wang Y, Zhong S, Jia Y, et al. Interhemispheric resting state functional connectivity abnormalities in unipolar depression and bipolar depression. Bipolar Disord 2015; 17:486-95.
88. Mulders PC, van Eijndhoven PF, Schene AH, Beckmann CF, Tendolkar I. Resting-state functional connectivity in major depressive disorder: a review. Neurosci Biobehav Rev 2015; 56:330-44.
89. Kyle SD, Beattie L, Spiegelhalder K, Rogers Z, Espie CA. Altered emotion perception in insomnia disorder. Sleep 2014; 37:775-83.
90. Holbrook AM, Crowther R, Lotter A, Cheng C, King D. The diagnosis and management of insomnia in clinical practice: a practical evidence based approach. CMAJ 2000; 162:216-20.
91. Morin CM, Culbert JP, Schwartz SM. Nonpharmacological interventions for insomnia: a meta-analysis of treatment efficacy. Am J Psychiatry 1994; 151:1172-80.
92. Ong JC, Manber R, Segal Z, Xia Y, Shapiro S, Wyatt JK. A randomized controlled trial of mindfulness meditation for chronic insomnia. Sleep 2014; 37:1553-63.
93. Jiang CG, Zhang T, Yue FG, Yi ML, Gao D. Efficacy of repetitive transcranial magnetic stimulation in the treatment of patients with chronic primary insomnia. Cell Biochem Biophys 2013; 67:169-73.
94. Buchsbaum MS, Gillin JC, Wu J, et al. Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sci 1989; 45:1349-56.
95. Heiss WD, Pawlik G, Herholz K, Wagner R, Wienhard K. Regional cerebral glucose metabolism in man during wakefulness, sleep, and dreaming. Brain Res 1985; 327:362-6.
96. Bastien CH Insomnia: Neurophysiological and neuropsychological approaches. Neuropsychol Rev 2011; 21:22-40.
97. Krueger JM, Huang YH, Rector DM, Buysse DJ. Sleep: a synchrony of cell activity-driven small network states. Eur J Neurosci 2013; 38:2199-209.
98. Kay DB, Soehner AM, Hasler BP, et al. Neurobiological basis for insomnia disorder: smaller wake-NREM sleep reductions in regional brain glucose metabolism compared to good sleepers. Sleep 2015; 38 (Abstract Suppl):A242-3.