Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T08:09:32.218Z Has data issue: false hasContentIssue false
  • English
  • Français

Sleep deprivation amplifies striatal activation to monetary reward

Published online by Cambridge University Press:  04 January 2013

B. C. Mullin ,
M. L. Phillips ,
G. J. Siegle ,
D. J. Buysse ,
E. E. Forbes  and
P. L. Franzen
B. C. Mullin
Affiliation:
Department of Psychiatry and Behavioral Sciences, Children's Hospital Colorado, Aurora, CO, USA
M. L. Phillips
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA Department of Psychological Medicine, Cardiff University, Cardiff, UK
G. J. Siegle
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
D. J. Buysse
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
E. E. Forbes
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
P. L. Franzen*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
*
*Address for correspondence: P. L. Franzen, Ph.D., Department of Psychiatry, University of Pittsburgh School of Medicine, 3811 O'Hara Street E-1119, Pittsburgh, PA 15213, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Sleep loss produces abnormal increases in reward seeking but the mechanisms underlying this phenomenon are poorly understood. The present study examined the influence of one night of sleep deprivation on neural responses to a monetary reward task in a sample of late adolescents/young adults.

Method

Using a within-subjects crossover design, 27 healthy, right-handed late adolescents/young adults (16 females, 11 males; mean age 23.1 years) underwent functional magnetic resonance imaging (fMRI) following a night of sleep deprivation and following a night of normal sleep. Participants' recent sleep history was monitored using actigraphy for 1 week prior to each sleep condition.

Results

Following sleep deprivation, participants exhibited increased activity in the ventral striatum (VS) and reduced deactivation in the medial prefrontal cortex (mPFC) during the winning of monetary reward, relative to the same task following normal sleep conditions. Shorter total sleep time over the five nights before the sleep-deprived testing condition was associated with reduced deactivation in the mPFC during reward.

Conclusions

These findings support the hypothesis that sleep loss produces aberrant functioning in reward neural circuitry, increasing the salience of positively reinforcing stimuli. Aberrant reward functioning related to insufficient sleep may contribute to the development and maintenance of reward dysfunction-related disorders, such as compulsive gambling, eating, substance abuse and mood disorders.

Keywords

Functional magnetic resonance imagingrewardsleepsleep deprivation
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 10 , October 2013 , pp. 2215 - 2225
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aalto, J, Kiianmaa, K (1986). REM-sleep deprivation-induced increase in ethanol intake: role of brain monoaminergic neurons. Alcohol 3, 377–381.CrossRefGoogle ScholarPubMed
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text revision (DSM-IV-TR). American Psychiatric Association: Washington, DC.Google Scholar
Berridge, KC, Kringelbach, ML (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457–480.CrossRefGoogle ScholarPubMed
Brower, KJ, Aldrich, MS, Hall, JM (1998). Polysomnographic and subjective sleep predictors of alcoholic relapse. Alcoholism, Clinical and Experimental Research 22, 1864–1871.CrossRefGoogle ScholarPubMed
Chee, MWL, Choo, WC (2004). Functional imaging of working memory after 24 hr of total sleep deprivation. Journal of Neuroscience 24, 4560–4567.CrossRefGoogle ScholarPubMed
Chee, MWL, Tan, JC, Zheng, H, Parimal, S, Weissman, DH, Zagorodnov, V, Dinges, DF (2008). Lapsing during sleep deprivation is associated with distributed changes in brain activation. Journal of Neuroscience 28, 5519–5528.CrossRefGoogle ScholarPubMed
Chuah, LYM, Dolcos, F, Chen, AK, Zheng, H, Parimal, S, Chee, MWL (2010). Sleep deprivation and interference by emotional distracters. Sleep 33, 1305–1313.CrossRefGoogle ScholarPubMed
Colombo, C, Benedetti, F, Barbini, B, Campori, E, Smeraldi, E (1999). Rate of switch from depression into mania after therapeutic sleep deprivation in bipolar depression. Psychiatric Research 86, 267–270.CrossRefGoogle ScholarPubMed
Delgado, MR, Nystrom, LE, Fissell, C, Noll, DC, Fiez, JA (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology 84, 3072–3077.CrossRefGoogle ScholarPubMed
Di Martino, A, Scheres, A, Margulies, DS, Kelly, A, Uddin, LQ, Shehzad, Z, Biswal, B, Walters, JR, Castellanos, FX, Milham, MP (2008). Functional connectivity of human striatum: a resting state fMRI study. Cerebral Cortex 18, 2735–2747.CrossRefGoogle ScholarPubMed
Drummond, SP, Brown, GG, Gillin, JC, Stricker, JL, Wong, EC, Buxton, RB (2000). Altered brain response to verbal learning following sleep deprivation. Nature 403, 655–657.CrossRefGoogle ScholarPubMed
Drummond, SP, Brown, GG, Stricker, JL, Buxton, RB, Wong, EC, Gillin, JC (1999). Sleep deprivation-induced reduction in cortical functional response to serial subtraction. Neuroreport 10, 3745–3748.CrossRefGoogle ScholarPubMed
Drummond, SP, Meloy, MJ, Yanagi, MA, Orff, HJ, Brown, GG (2005). Compensatory recruitment after sleep deprivation and the relationship with performance. Psychiatry Research 140, 211–223.CrossRefGoogle ScholarPubMed
Ernst, M, Nelson, EE, Jazbec, S, McClure, EB, Monk, CS, Leibenluft, E, Blair, J, Pine, DS (2005). Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. NeuroImage 25, 1279–1291.CrossRefGoogle ScholarPubMed
Ernst, M, Nelson, EE, McClure, EB, Monk, CS, Munson, S, Eshel, N, Zarahn, E, Leibenluft, E, Zametkin, A, Towbin, K, Blair, J, Charney, D, Pine, DS (2004). Choice selection and reward anticipation: an fMRI study. Neuropsychologia 42, 1585–1597.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1995). Structured Clinical Interview for DSM-IV Axis I Disorders, Version 2.0. Biometric Research Department, New York State Psychiatric Institute: New York.Google Scholar
Forbes, EE, Brown, SM, Kimak, M, Ferrell, RE, Manuck, SB, Hariri, AR (2009). Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity. Molecular Psychiatry 14, 60–70.CrossRefGoogle ScholarPubMed
Forbes, EE, Dahl, RE (2012). Research review: Altered reward function in adolescent depression: what, when and how? Journal of Child Psychology and Psychiatry 53, 3–15.CrossRefGoogle ScholarPubMed
Forbes, EE, Olino, TM, Ryan, ND, Birmaher, B, Axelson, D, Moyles, DL, Dahl, RE (2010). Reward-related brain function as a predictor of treatment response in adolescents with major depressive disorder. Cognitive, Affective, and Behavioral Neuroscience 10, 107–118.CrossRefGoogle ScholarPubMed
Franzen, PL, Buysse, DJ, Dahl, RE, Thompson, W, Siegle, GJ (2009). Sleep deprivation alters pupillary reactivity to emotional stimuli in healthy young adults. Biological Psychology 80, 300–305.CrossRefGoogle ScholarPubMed
Franzen, PL, Buysse, DJ, Duryea, DN, Wood, A, Siegle, GJ, Dahl, RE (2010). The emotional impact of sleep restriction in adolescents. Sleep 33S, A85.Google Scholar
Goel, N, Rao, H, Durmer, JS, Dinges, DF (2009). Neurocognitive consequences of sleep deprivation. Seminars in Neurology 29, 320–339.CrossRefGoogle ScholarPubMed
Goodwin, FK, Jamison, KR (2007). Manic-Depressive Illness: Bipolar Disorders and Recurrent Depression, 2nd edn.Oxford University Press: New York.Google Scholar
Grandner, MA, Patel, NP, Gehrman, PR, Perlis, ML, Pack, AI (2010). Problems associated with short sleep: bridging the gap between laboratory and epidemiological studies. Sleep Medicine Reviews 14, 239–247.CrossRefGoogle Scholar
Gujar, N, Yoo, SS, Hu, P, Walker, MP (2010). The unrested resting brain: sleep deprivation alters activity within the default-mode network. Journal of Cognitive Neuroscience 22, 1637–1648.CrossRefGoogle ScholarPubMed
Gujar, N, Yoo, SS, Hu, P, Walker, MP (2011). Sleep deprivation amplifies reactivity of brain reward networks, biasing the appraisal of positive emotional experiences. Journal of Neuroscience 31, 4466–4474.CrossRefGoogle ScholarPubMed
Haber, SN, Knutson, B (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.CrossRefGoogle ScholarPubMed
Jackson, A, Cavanagh, J, Scott, J (2003). A systematic review of manic and depressive prodromes. Journal of Affective Disorders 74, 209–217.CrossRefGoogle ScholarPubMed
Kessler, RC, Berglund, P, Demler, O, Jin, R, Merikangas, KR, Walters, EE (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 62, 593–602.CrossRefGoogle ScholarPubMed
Kirsch, P, Schienle, A, Stark, R, Sammer, G, Blecker, C, Walter, B, Ott, U, Burkart, J, Vaitl, D (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20, 1086–1095.CrossRefGoogle Scholar
Knutson, B, Adams, CM, Fong, GW, Hommer, D (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience 21, RC159.CrossRefGoogle ScholarPubMed
Liu, X, Powell, DK, Wang, H, Gold, BT, Corbly, CR, Joseph, JE (2007). Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. Journal of Neuroscience 27, 4587–4597.CrossRefGoogle ScholarPubMed
Mason, MF, Norton, MI, Van Horn, JD, Wegner, DM, Grafton, ST, Macrae, CN (2007). Wandering minds: the default network and stimulus-independent thought. Science 315, 393–395.CrossRefGoogle ScholarPubMed
McKenna, BS, Dickinson, DL, Orff, HJ, Drummond, SP (2007). The effects of one night of sleep deprivation on known-risk and ambiguous-risk decisions. Journal of Sleep Research 16, 245–252.CrossRefGoogle ScholarPubMed
Millman, R (2005). Excessive sleepiness in adolescents and young adults: causes, consequences, and treatment strategies. Pediatrics 115, 1774–1786.CrossRefGoogle Scholar
Mini Mitter Co. Inc. (2001). Actiwatch 16/Actiwatch 64/Actiwatch L/Actiwatch-Score Instruction Manual. Mini Mitter Co. Inc.; Bend, OR.Google Scholar
Morgenthaler, T, Alessi, C, Friedman, L, Owens, J, Kapur, V, Boehlecke, B, Brown, T, Chesson, A, Coleman, J, Lee-Chiong, T, Pancer, J, Swick, TJ (2007). Practice parameters for the use of actigraphy in the assessment of sleep and sleep disorders: an update for 2007. Sleep 30, 519–529.CrossRefGoogle ScholarPubMed
Mu, Q, Nahas, Z, Johnson, KA, Yamanaka, K, Mishory, A, Koola, J, Hill, S, Horner, MD, Bohning, DE, George, MS (2005). Decreased cortical response to verbal working memory following sleep deprivation. Sleep 28, 55–67.CrossRefGoogle ScholarPubMed
Nedeltcheva, AV, Kilkus, JM, Imperial, J, Kasza, K, Schoeller, DA, Penev, PD (2009). Sleep curtailment is accompanied by increased intake of calories from snacks. American Journal of Clinical Nutrition 89, 126–133.CrossRefGoogle ScholarPubMed
O'Doherty, JP (2004). Reward representations and reward-related learning in the human brain: insights from neuroimaging. Current Opinion in Neurobiology 14, 769–776.CrossRefGoogle ScholarPubMed
O'Doherty, JP, Deichmann, R, Critchley, HD, Dolan, RJ (2002). Neural responses during anticipation of a primary taste reward. Neuron 33, 815–826.CrossRefGoogle ScholarPubMed
Philip, P, Taillard, J, Sagaspe, P, Valtat, C, Sanchez-Ortuno, M, Moore, N, Charles, A, Bioulac, B (2004). Age, performance and sleep deprivation. Journal of Sleep Research 13, 105–110.CrossRefGoogle ScholarPubMed
Phillips, ML, Ladouceur, CD, Drevets, WC (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833–857.CrossRefGoogle ScholarPubMed
Postuma, RB, Dagher, A (2006). Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cerebral Cortex 16, 1508–1521.CrossRefGoogle ScholarPubMed
Puhl, MD, Fang, J, Grigson, PS (2009). Acute sleep deprivation increases the rate and efficiency of cocaine self-administration, but not the perceived value of cocaine reward in rats. Pharmacology Biochemistry and Behavior 94, 262–270.CrossRefGoogle Scholar
Rademacher, L, Krach, S, Kohls, G, Irmak, A, Gründer, G, Spreckelmeyer, KN (2010). Dissociation of neural networks for anticipation and consumption of monetary and social rewards. NeuroImage 49, 3276–3285.CrossRefGoogle ScholarPubMed
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 676–682.CrossRefGoogle ScholarPubMed
Respironics Inc. (2011). Actiwatch Communication and Sleep Analysis Software. Respironics Inc.: Murrysville, PA.Google Scholar
Spreckelmeyer, KN, Krach, S, Kohls, G, Rademacher, L, Irmak, A, Konrad, K, Kircher, T, Gründer, G (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience 4, 158–165.CrossRefGoogle ScholarPubMed
Steptoe, A, Peacey, V, Wardle, J (2006). Sleep duration and health in young adults. Archives of Internal Medicine 166, 1689–1692.CrossRefGoogle ScholarPubMed
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 (2000). Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. Journal of Sleep Research 9, 335–352.CrossRefGoogle Scholar
Thomas, ML, Sing, HC, Belenky, G, Holcomb, HH, Mayberg, HS, Dannals, RF, Wagner, HN, Thorne, DR, Popp, KA, Rowland, LM, Welsh, AB, Balwinski, SM, Redmond, DP (2003). Neural basis of alertness and cognitive performance impairments during sleepiness. II. Effects of 48 and 72 h of sleep deprivation on waking human regional brain activity. Thalamus and Related Systems 2, 199–229.Google Scholar
Tomasi, D, Wang, RL, Telang, F, Boronikolas, V, Jayne, MC, Wang, GJ, Fowler, JS, Volkow, ND (2009). Impairment of attentional networks after 1 night of sleep deprivation. Cerebral Cortex 19, 233–240.CrossRefGoogle ScholarPubMed
Uddin, LQ, Iacoboni, M, Lange, C, Keenan, JP (2007). The self and social cognition: the role of cortical midline structures and mirror neurons. Trends in Cognitive Sciences 11, 153–157.CrossRefGoogle ScholarPubMed
Van Leijenhorst, L, Zanolie, K, Van Meel, CS, Westenberg, PM, Rombouts, S, Crone, EA (2010). What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cerebral Cortex 20, 61–69.CrossRefGoogle ScholarPubMed
Venkatraman, V, Chuah, LYM, Huettel, SA, Chee, MWL (2007). Sleep deprivation elevates expectation of gains and attenuates response to losses following risky decisions. Sleep 30, 603–609.CrossRefGoogle ScholarPubMed
Venkatraman, V, Huettel, SA, Chuah, LYM, Payne, JW, Chee, MWL (2011). Sleep deprivation biases the neural mechanisms underlying economic preferences. Journal of Neuroscience 31, 3712–3718.CrossRefGoogle ScholarPubMed
Volkow, ND, Tomasi, D, Wang, G, Telang, F, Fowler, JS, Wang, RL, Logan, J, Wong, C, Jayne, M, Swanson, JM (2009). Hyperstimulation of striatal D2 receptors with sleep deprivation: Implications for cognitive impairment. NeuroImage 45, 1232–1240.CrossRefGoogle ScholarPubMed
Ward, BD (2000). Simultaneous inference for fMRI data (http://afni.nimh.nih.gov/pub/dist/doc/manual/AlphaSim.pdf). Accessed 1 March 2011.Google Scholar
Wu, JC, Gillin, JC, Buchsbaum, MS, Chen, P, Keator, DB, Wu, NK, Darnall, LA, Fallon, JH, Bunney, WE (2006). Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 31, 2783–2792.CrossRefGoogle Scholar
Wu, JC, Gillin, JC, Buchsbaum, MS, Hershey, T, Hazlett, E, Sicotte, N, Bunney, WE (1991). The effect of sleep deprivation on cerebral glucose metabolic rate in normal humans assessed with positron emission tomography. Sleep 14, 155–162.Google ScholarPubMed
Yoo, SS, Gujar, N, Hu, P, Jolesz, FA, Walker, MP (2007). The human emotional brain without sleep – a prefrontal amygdala disconnect. Current Biology 23, 88–89.Google Scholar