Daytime sleepiness affects prefrontal regulation of food intake

NeuroImage

Volumn 71, Issue , 2013, Pages 216-223

  Killgore, William D S ^a   Schwab, Zachary J ^a   Weber, Mareen ^a   Kipman, Maia ^a   DelDonno, Sophie R ^a   Weiner, Melissa R ^a   Rauch, Scott L ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

Appetite; FMRI; Food; Neuroimaging; Prefrontal cortex; Sex differences; Sleep; Sleepiness

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; DAYTIME SOMNOLENCE; EPWORTH SLEEPINESS SCALE; FEMALE; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; INCREASED APPETITE; MALE; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; SEX DIFFERENCE; VENTROMEDIAL PREFRONTAL CORTEX;

ADOLESCENT; ADULT; BRAIN MAPPING; EATING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; SEX CHARACTERISTICS; SLEEP; YOUNG ADULT;

EID: 84873729215     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.01.018     Document Type: Article

References (79)

1. Bechara A. The role of emotion in decision-making: evidence from neurological patients with orbitofrontal damage. Brain Cogn. 2004, 55:30-40.
2. Bechara A., Damasio A.R., Damasio H., Anderson S.W. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 1994, 50:7-15.
3. Bechara A., Damasio H., Damasio A.R. Emotion, decision making and the orbitofrontal cortex. Cereb. Cortex 2000, 10:295-307.
4. Benedict C., Brooks S.J., O'Daly O.G., Almen M.S., Morell A., Aberg K., Gingnell M., Schultes B., Hallschmid M., Broman J.E., Larsson E.M., Schioth H.B. Acute sleep deprivation enhances the brain's response to hedonic food stimuli: an fMRI study. J. Clin. Endocrinol. Metab. 2012, 97:E443-E447.
5. Blasi G., Goldberg T.E., Weickert T., Das S., Kohn P., Zoltick B., Bertolino A., Callicott J.H., Weinberger D.R., Mattay V.S. Brain regions underlying response inhibition and interference monitoring and suppression. Eur. J. Neurosci. 2006, 23:1658-1664.
6. Brondel L., Romer M.A., Nougues P.M., Touyarou P., Davenne D. Acute partial sleep deprivation increases food intake in healthy men. Am. J. Clin. Nutr. 2010, 91:1550-1559.
7. Center for Disease Control and Prevention Short sleep duration among workers-United States, 2010. Morbidity and Mortality Weekly Report 2012, 281-285. U.S. Government Printing Office, Washington.
8. Cornier M.A., Salzberg A.K., Endly D.C., Bessesen D.H., Tregellas J.R. Sex-based differences in the behavioral and neuronal responses to food. Physiol. Behav. 2010, 99:538-543.
9. De Havas J.A., Parimal S., Soon C.S., Chee M.W. Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. NeuroImage 2012, 59:1745-1751.
10. Doallo S., Raymond J.E., Shapiro K.L., Kiss M., Eimer M., Nobre A.C. Response inhibition results in the emotional devaluation of faces: neural correlates as revealed by fMRI. Soc. Cogn. Affect. Neurosci. 2012, 7:649-659.
11. Drake C.L. Subjective measures of sleepiness. Sleepiness: Causes, Consequence and Treatment 2011, 60-71. Cambridge University Press, New York. M.J. Thorpy, M. Billiard (Eds.).
12. Drummond S.P., Paulus M.P., Tapert S.F. Effects of two nights sleep deprivation and two nights recovery sleep on response inhibition. J. Sleep Res. 2006, 15:261-265.
13. Flegal K.M., Carroll M.D., Ogden C.L., Johnson C.L. Prevalence and trends in obesity among US adults, 1999-2000. JAMA 2002, 288:1723-1727.
14. Frank S., Laharnar N., Kullmann S., Veit R., Canova C., Hegner Y.L., Fritsche A., Preissl H. Processing of food pictures: influence of hunger, gender and calorie content. Brain Res. 2010, 1350:159-166.
15. Gale S.M., Castracane V.D., Mantzoros C.S. Energy homeostasis, obesity and eating disorders: recent advances in endocrinology. J. Nutr. 2004, 134:295-298.
16. Gallup Organization Sleep in America 1995.
17. Gangwisch J.E., Malaspina D., Boden-Albala B., Heymsfield S.B. Inadequate sleep as a risk factor for obesity: analyses of the NHANES I. Sleep 2005, 28:1289-1296.
18. Hariri A.R., Mattay V.S., Tessitore A., Fera F., Weinberger D.R. Neocortical modulation of the amygdala response to fearful stimuli. Biol. Psychiatry 2003, 53:494-501.
19. Harrison Y., Horne J.A. The impact of sleep deprivation on decision making: a review. J. Exp. Psychol. Appl. 2000, 6:236-249.
20. Hasler G., Buysse D.J., Klaghofer R., Gamma A., Ajdacic V., Eich D., Rossler W., Angst J. The association between short sleep duration and obesity in young adults: a 13-year prospective study. Sleep 2004, 27:661-666.
21. Hodgson T.L., Mort D., Chamberlain M.M., Hutton S.B., O'Neill K.S., Kennard C. Orbitofrontal cortex mediates inhibition of return. Neuropsychologia 2002, 40:1891-1901.
22. Hoek H.W. Incidence, prevalence and mortality of anorexia nervosa and other eating disorders. Curr. Opin. Psychiatry 2006, 19:389-394.
23. Hornberger M., Geng J., Hodges J.R. Convergent grey and white matter evidence of orbitofrontal cortex changes related to disinhibition in behavioural variant frontotemporal dementia. Brain 2011, 134:2502-2512.
24. Johns M.W. A new method for measuring daytime sleepiness: the Epworth Sleepiness Scale. Sleep 1991, 14:540-545.
25. Johns M.W. Reliability and factor analysis of the Epworth Sleepiness Scale. Sleep 1992, 15:376-381.
26. Killgore W.D.S. Effects of sleep deprivation and morningness-eveningness traits on risk-taking. Psychol. Rep. 2007, 100:613-626.
27. Killgore W.D.S. Effects of sleep deprivation on cognition. Prog. Brain Res. 2010, 185:105-129.
28. Killgore W.D.S., Yurgelun-Todd D.A. Body mass predicts orbitofrontal activity during visual presentations of high-calorie foods. Neuroreport 2005, 16:859-863.
29. Killgore W.D.S., Yurgelun-Todd D.A. Developmental changes in the functional brain responses of adolescents to images of high and low-calorie foods. Dev. Psychobiol. 2005, 47:377-397.
30. Killgore W.D.S., Yurgelun-Todd D.A. Affect modulates appetite-related brain activity to images of food. Int. J. Eat. Disord. 2006, 39:357-363.
31. Killgore W.D.S., Yurgelun-Todd D.A. Positive affect modulates activity in the visual cortex to images of high calorie foods. Int. J. Neurosci. 2007, 117:643-653.
32. Killgore W.D.S., Yurgelun-Todd D.A. Sex differences in cerebral responses to images of high versus low-calorie food. Neuroreport 2010, 21:354-358.
33. Killgore W.D.S., Young A.D., Femia L.A., Bogorodzki P., Rogowska J., Yurgelun-Todd D.A. Cortical and limbic activation during viewing of high- versus low-calorie foods. NeuroImage 2003, 19:1381-1394.
34. Killgore W.D.S., Balkin T.J., Wesensten N.J. Impaired decision-making following 49hours of sleep deprivation. J. Sleep Res. 2006, 15:7-13.
35. Killgore W.D.S., Ross A.J., Kamiya T., Kawada Y., Renshaw P.F., Yurgelun-Todd D.A. Citicoline affects appetite and cortico-limbic responses to images of high-calorie foods. Int. J. Eat. Disord. 2010, 43:6-13.
36. Killgore W.D., Kamimori G.H., Balkin T.J. Caffeine protects against increased risk-taking propensity during severe sleep deprivation. J. Sleep Res. 2011, 20:395-403.
37. Killgore W.D., Grugle N.L., Balkin T.J. Gambling when sleep deprived: don't bet on stimulants. Chronobiol. Int. 2012, 29:43-54.
38. Killgore W.D., Schwab Z.J., Kipman M., Deldonno S.R., Weber M. Voxel-based morphometric gray matter correlates of daytime sleepiness. Neurosci. Lett. 2012, 518:10-13.
39. Killgore W.D., Schwab Z.J., Weiner M.R. Self-reported nocturnal sleep duration is associated with next-day resting state functional connectivity. Neuroreport 2012, 23:741-745.
40. Knutson K.L., Spiegel K., Penev P., Van Cauter E. The metabolic consequences of sleep deprivation. Sleep Med. Rev. 2007, 11:163-178.
41. Kripke D.F., Simons R.N., Garfinkel L., Hammond E.C. Short and long sleep and sleeping pills. Is increased mortality associated?. Arch. Gen. Psychiatry 1979, 36:103-116.
42. Lewinsohn P.M., Seeley J.R., Moerk K.C., Striegel-Moore R.H. Gender differences in eating disorder symptoms in young adults. Int. J. Eat. Disord. 2002, 32:426-440.
43. Libedinsky C., Smith D.V., Teng C.S., Namburi P., Chen V.W., Huettel S.A., Chee M.W. Sleep deprivation alters valuation signals in the ventromedial prefrontal cortex. Front. Behav. Neurosci. 2011, 5:70.
44. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003, 19:1233-1239.
45. McKenna B.S., Dickinson D.L., Orff H.J., Drummond S.P. The effects of one night of sleep deprivation on known-risk and ambiguous-risk decisions. J. Sleep Res. 2007, 16:245-252.
46. Middelkoop H.A., Smilde-van den Doel D.A., Neven A.K., Kamphuisen H.A., Springer C.P. Subjective sleep characteristics of 1,485 males and females aged 50-93: effects of sex and age, and factors related to self-evaluated quality of sleep. J. Gerontol. A Biol. Sci. Med. Sci. 1996, 51:M108-M115.
47. National Sleep Foundation Sleep in America Poll 2005, National Sleep Foundation, Washington.
48. National Sleep Foundation Sleep in America Poll 2007, National Sleep Foundation, Washington.
49. Nedeltcheva A.V., Kilkus J.M., Imperial J., Kasza K., Schoeller D.A., Penev P.D. Sleep curtailment is accompanied by increased intake of calories from snacks. Am. J. Clin. Nutr. 2009, 89:126-133.
50. O'Connor C., Thornley K.S., Hanly P.J. Gender differences in the polysomnographic features of obstructive sleep apnea. Am. J. Respir. Cri.t Care Med. 2000, 161:1465-1472.
51. Ogden C.L., Carroll M.D., Curtin L.R., McDowell M.A., Tabak C.J., Flegal K.M. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 2006, 295:1549-1555.
52. Ogden C.L., Carroll M.D., Kit B.K., Flegal K.M. Prevalence of obesity in the United States, 2009-2010. NCHS data brief 2012, 1-8.
53. Patel S.R. Reduced sleep as an obesity risk factor. Obes. Rev. 2009, 10(Suppl. 2):61-68.
54. Patel S.R., Hu F.B. Short sleep duration and weight gain: a systematic review. Obesity 2008, 16:643-653.
55. Patel S.R., Blackwell T., Redline S., Ancoli-Israel S., Cauley J.A., Hillier T.A., Lewis C.E., Orwoll E.S., Stefanick M.L., Taylor B.C., Yaffe K., Stone K.L. The association between sleep duration and obesity in older adults. Int. J. Obes. 2008, 32:1825-1834.
56. Paulus M.P., Frank L.R. Ventromedial prefrontal cortex activation is critical for preference judgments. Neuroreport 2003, 14:1311-1315.
57. Pejovic S., Vgontzas A.N., Basta M., Tsaoussoglou M., Zoumakis E., Vgontzas A., Bixler E.O., Chrousos G.P. Leptin and hunger levels in young healthy adults after one night of sleep loss. J. Sleep Res. 2010, 19:552-558.
58. Pilcher J.J., Pury C.L., Muth E.R. Assessing subjective daytime sleepiness: an internal state versus behavior approach. Behav. Med. 2003, 29:60-67.
59. Rechtschaffen A., Bergmann B.M. Sleep deprivation in the rat by the disk-over-water method. Behav. Brain Res. 1995, 69:55-63.
60. Ridderinkhof K.R., van den Wildenberg W.P., Segalowitz S.J., Carter C.S. Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn. 2004, 56:129-140.
61. Samann P.G., Tully C., Spoormaker V.I., Wetter T.C., Holsboer F., Wehrle R., Czisch M. Increased sleep pressure reduces resting state functional connectivity. MAGMA 2010, 23:375-389.
62. Silbersweig D., Clarkin J.F., Goldstein M., Kernberg O.F., Tuescher O., Levy K.N., Brendel G., Pan H., Beutel M., Pavony M.T., Epstein J., Lenzenweger M.F., Thomas K.M., Posner M.I., Stern E. Failure of frontolimbic inhibitory function in the context of negative emotion in borderline personality disorder. Am. J. Psychiatry 2007, 164:1832-1841.
63. Spiegel K., Tasali E., Penev P., Van Cauter E. Brief communication: Sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann. Intern. Med. 2004, 141:846-850.
64. Striegel-Moore R.H., Bulik C.M. Risk factors for eating disorders. Am. Psychol. 2007, 62:181-198.
65. Striegel-Moore R.H., Rosselli F., Perrin N., DeBar L., Wilson G.T., May A., Kraemer H.C. Gender difference in the prevalence of eating disorder symptoms. Int. J. Eat. Disord. 2009, 42:471-474.
66. Szatkowska I., Szymanska O., Bojarski P., Grabowska A. Cognitive inhibition in patients with medial orbitofrontal damage. Exp. Brain Res. 2007, 181:109-115.
67. Taheri S., Lin L., Austin D., Young T., Mignot E. Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med. 2004, 1:e62.
68. Thomas M., Sing H., Belenky G., Holcomb H., Mayberg H., Dannals R., Wagner H., Thorne D., Popp K., Rowland L., Welsh A., Balwinski S., Redmond D. Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24h of sleep deprivation on waking human regional brain activity. J. Sleep Res. 2000, 9:335-352.
69. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
70. Van Cauter E., Knutson K.L. Sleep and the epidemic of obesity in children and adults. Eur. J. Endocrinol. 2008, 159(Suppl. 1):S59-S66.
71. Van Cauter E., Spiegel K., Tasali E., Leproult R. Metabolic consequences of sleep and sleep loss. Sleep Med. 2008, 9(Suppl. 1):S23-S28.
72. van der Lely A.J., Tschop M., Heiman M.L., Ghigo E. Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr. Rev. 2004, 25:426-457.
73. Venkatraman V., Chuah Y.M., Huettel S.A., Chee M.W. Sleep deprivation elevates expectation of gains and attenuates response to losses following risky decisions. Sleep 2007, 30:603-609.
74. Venkatraman V., Huettel S.A., Chuah L.Y., Payne J.W., Chee M.W. Sleep deprivation biases the neural mechanisms underlying economic preferences. J. Neurosci. 2011, 31:3712-3718.
75. Wang G.J., Volkow N.D., Telang F., Jayne M., Ma Y., Pradhan K., Zhu W., Wong C.T., Thanos P.K., Geliebter A., Biegon A., Fowler J.S. Evidence of gender differences in the ability to inhibit brain activation elicited by food stimulation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1249-1254.
76. Woods S.C., Gotoh K., Clegg D.J. Gender differences in the control of energy homeostasis. Exp. Biol. Med. 2003, 228:1175-1180.
77. Wu J.C., Gillin J.C., Buchsbaum M.S., Chen P., Keator D.B., Khosla Wu N., Darnall L.A., Fallon J.H., Bunney W.E. Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 2006, 31:2783-2792.
78. Yoo S.S., Gujar N., Hu P., Jolesz F.A., Walker M.P. The human emotional brain without sleep-a prefrontal amygdala disconnect. Curr. Biol. 2007, 17:R877-R878.
79. Zhang B., Wing Y.K. Sex differences in insomnia: a meta-analysis. Sleep 2006, 29:85-93.