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Experimentally imposed circadian misalignment alters the neural response to monetary rewards and response inhibition in healthy adolescents

Published online by Cambridge University Press:  17 March 2021

Brant P. Hasler Open the ORCID record for Brant P. Hasler [Opens in a new window] ,
Adriane M. Soehner ,
Meredith L. Wallace ,
Ryan W. Logan ,
Wambui Ngari ,
Erika E. Forbes ,
Daniel J. Buysse  and
Duncan B. Clark
Brant P. Hasler*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Adriane M. Soehner
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Meredith L. Wallace
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Ryan W. Logan
Affiliation:
Department of Pharmacology and Experimental Therapeutics, Boston University School of Medicine, Boston, MA, USA
Wambui Ngari
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Erika E. Forbes
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Daniel J. Buysse
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Duncan B. Clark
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
*
Author for correspondence: Brant P. Hasler, E-mail: [email protected]
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Abstract

Background

Sleep and circadian timing shifts later during adolescence, conflicting with early school start times, and resulting in circadian misalignment. Although circadian misalignment has been linked to depression, substance use, and altered reward function, a paucity of experimental studies precludes the determination of causality. Here we tested, for the first time, whether experimentally-imposed circadian misalignment alters the neural response to monetary reward and/or response inhibition.

Methods

Healthy adolescents (n = 25, ages 13–17) completed two in-lab sleep schedules in counterbalanced order: An ‘aligned’ condition based on typical summer sleep-wake times (0000–0930) and a ‘misaligned’ condition mimicking earlier school year sleep-wake times (2000–0530). Participants completed morning and afternoon functional magnetic resonance imaging scans during each condition, including monetary reward (morning only) and response inhibition (morning and afternoon) tasks. Total sleep time and circadian phase were assessed via actigraphy and salivary melatonin, respectively.

Results

Bilateral ventral striatal (VS) activation during reward outcome was lower during the Misaligned condition after accounting for the prior night's total sleep time. Bilateral VS activation during reward anticipation was lower during the Misaligned condition, including after accounting for covariates, but did not survive correction for multiple comparisons. Right inferior frontal gyrus activation during response inhibition was lower during the Misaligned condition, before and after accounting for total sleep time and vigilant attention, but only during the morning scan.

Conclusions

Our findings provide novel experimental evidence that circadian misalignment analogous to that resulting from school schedules may have measurable impacts on healthy adolescents' reward processing and inhibition of prepotent responses.

Keywords

Adolescentscircadian rhythmsfMRIrewardimpulse controlsleep
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 16 , December 2022 , pp. 3939 - 3947
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Alonso, I., Pino, J., Kortagere, S., Torres, G., & Espana, R. (2021). Dopamine transporter function fluctuates across sleep/wake state: Potential impact for addiction. Neuropsychopharmacology, 46, 699–708.CrossRefGoogle ScholarPubMed
American Academy of Sleep Medicine. (2014). International classification of sleep disorders–third edition (ICSD-3). Darien, IL: American Academy of Sleep Medicine.Google Scholar
Ancold, A., & Stephen, C. (1995). Development of a short questionnaire for use in epidemiological studies of depression in children and adolescents. International Journal of Methods in Psychiatric Research, 5, 237–249.Google Scholar
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116.CrossRefGoogle ScholarPubMed
Ashburner, J., Barnes, G., Chen, C., Daunizeau, J., Flandin, G., Friston, K., … Moran, R. (2014). SPM12 manual. Wellcome Trust Centre for Neuroimaging.Google Scholar
Balachandran, R. C., Hatcher, K., Sieg, M. L., Sullivan, E. K., Molina, L. M., Mahoney, M. M., & Eubig, P. A. (2020). Pharmacological challenges examining the underlying mechanism of altered response inhibition and attention due to circadian disruption in adult long-Evans rats. Pharmacology Biochemistry and Behavior, 193, 172915.CrossRefGoogle ScholarPubMed
Bari, A., & Robbins, T. W. (2013). Inhibition and impulsivity: Behavioral and neural basis of response control. Progress in Neurobiology, 108, 44–79.CrossRefGoogle ScholarPubMed
Benloucif, S., Burgess, H. J., Klerman, E. B., Lewy, A. J., Middleton, B., Murphy, P. J., … Revell, V. L. (2008). Measuring melatonin in humans. Journal of Clinical Sleep Medicine, 4, 66–69.CrossRefGoogle ScholarPubMed
Birmaher, B., Brent, D. A., Chiappetta, L., Bridge, J., Monga, S., & Baugher, M. (1999). Psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED): A replication study. Journal of the American Academy of Child & Adolescent Psychiatry, 38(10), 1230–1236.CrossRefGoogle ScholarPubMed
Bullock, B., Murray, G., Anderson, J., Cooper-O'Neill, T., Gooley, J., Cain, S., & Lockley, S. (2017). Constraint is associated with earlier circadian phase and morningness: Confirmation of relationships between personality and circadian phase using a constant routine protocol. Personality and Individual Differences, 104, 69–74.CrossRefGoogle ScholarPubMed
Byrne, J. E. M., Hughes, M. E., Rossell, S. L., Johnson, S. L., & Murray, G. (2017). Time of day differences in neural reward functioning in healthy young men. Journal of Neuroscience, 37, 8895–8900.CrossRefGoogle ScholarPubMed
Byrne, J. E., & Murray, G. (2017). Diurnal rhythms in psychological reward functioning in healthy young men: ‘Wanting’, liking, and learning. Chronobiology International, 34(2), 287–295.CrossRefGoogle ScholarPubMed
Caci, H., Mattei, V., Baylé, F. J., Nadalet, L., Dossios, C., Robert, P., & Boyer, P. (2005). Impulsivity but not venturesomeness is related to morningness. Psychiatry Research, 134(3), 259–265.CrossRefGoogle Scholar
Cao, J., & Zhang, S. (2014). Multiple comparison procedures. JAMA, 312(5), 543–544.CrossRefGoogle ScholarPubMed
Carlisi, C. O., Hilbert, K., Guyer, A. E., & Ernst, M. (2017). Sleep-amount differentially affects fear-processing neural circuitry in pediatric anxiety: A preliminary fMRI investigation. Cognitive, Affective, & Behavioral Neuroscience, 17(6), 1098–1113.CrossRefGoogle ScholarPubMed
Carney, C. E., Buysse, D. J., Ancoli-Israel, S., Edinger, J. D., Krystal, A. D., Lichstein, K. L., & Morin, C. M. (2012). The consensus sleep diary: Standardizing prospective sleep self-monitoring. Sleep, 35(2), 287–302.CrossRefGoogle ScholarPubMed
Casey, B., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., … Cohen, J. D. (1997). A developmental functional MRI study of prefrontal activation during performance of a go-no-go task. Journal of Cognitive Neuroscience, 9(6), 835–847.CrossRefGoogle ScholarPubMed
Chikazoe, J., Konishi, S., Asari, T., Jimura, K., & Miyashita, Y. (2007). Activation of right inferior frontal gyrus during response inhibition across response modalities. Journal of Cognitive Neuroscience, 19(1), 69–80.CrossRefGoogle ScholarPubMed
Crowley, S. J., Wolfson, A. R., Tarokh, L., & Carskadon, M. A. (2018). An update on adolescent sleep: New evidence informing the perfect storm model. Journal of Adolescence, 67, 55–65.CrossRefGoogle ScholarPubMed
Dorrian, J., Rogers, N. L., & Dinges, D. F. (2005). Psychomotor vigilance performance: Neurocognitive assay sensitive to sleep loss. In Kushida, C. (Ed.). Sleep deprivation (pp. 39–70). New York, NY: Marcel Dekker.Google Scholar
Elliott, M. L., Knodt, A. R., Ireland, D., Morris, M. L., Poulton, R., Ramrakha, S., … Hariri, A. R. (2020). What is the test-retest reliability of common task-functional MRI measures? New empirical evidence and a meta-analysis. Psychological Science, 31, 792–806.CrossRefGoogle ScholarPubMed
Emens, J. S., Yuhas, K., Rough, J., Kochar, N., Peters, D., & Lewy, A. J. (2009). Phase angle of entrainment in morning- and evening-types under naturalistic conditions. Chronobiology International, 26(3), 474–493.CrossRefGoogle ScholarPubMed
Forbes, E. E., & Dahl, R. E. (2012). Research review: Altered reward function in adolescent depression: What, when and how? Journal of Child Psychology and Psychiatry, 53(1), 3–15.CrossRefGoogle ScholarPubMed
Hampshire, A., Chamberlain, S. R., Monti, M. M., Duncan, J., & Owen, A. M. (2010). The role of the right inferior frontal gyrus: Inhibition and attentional control. NeuroImage, 50(3), 1313–1319.CrossRefGoogle ScholarPubMed
Hasler, B. P., Allen, J. J. B., Sbarra, D. A., Bootzin, R. R., & Bernert, R. A. (2010a). Morningness-eveningness and depression: Preliminary evidence for the role of BAS and positive affect. Psychiatry Research, 176(2–3), 166–173.CrossRefGoogle ScholarPubMed
Hasler, B. P., Bootzin, R. R., Cousins, J. C., Fridel, K., & Wenk, G. L. (2008a). Circadian phase in sleep-disturbed adolescents with a history of substance abuse: A pilot study. Behavioral Sleep Medicine, 6(1), 55–73.CrossRefGoogle ScholarPubMed
Hasler, B. P., Bruce, S., Scharf, D., Ngari, W., & Clark, D. B. (2019). Circadian misalignment and weekend alcohol use in late adolescent drinkers: Preliminary evidence. Chronobiology International, 36(6), 796–810.CrossRefGoogle ScholarPubMed
Hasler, B. P., Buysse, D. J., Kupfer, D. J., & Germain, A. (2010b). Phase relationships between core body temperature, melatonin, and sleep are associated with depression severity: Further evidence for circadian misalignment in non-seasonal depression. Psychiatry Research, 178(1), 205–207.CrossRefGoogle ScholarPubMed
Hasler, B. P., & Clark, D. B. (2013). Circadian misalignment, reward-related brain function, and adolescent alcohol involvement. Alcoholism: Clinical and Experimental Research, 37(4), 558–565.CrossRefGoogle ScholarPubMed
Hasler, B. P., Dahl, R. E., Holm, S. M., Jakubcak, J. L., Ryan, N. D., Silk, J. S., … Forbes, E. E. (2012). Weekend-weekday advances in sleep timing are associated with altered reward-related brain function in healthy adolescents. Biological Psychology, 91(3), 334–341.CrossRefGoogle ScholarPubMed
Hasler, B. P., Forbes, E. E., & Franzen, P. L. (2014). Time-of-day differences and short-term stability of the neural response to monetary reward: A pilot study. Psychiatry Research: Neuroimaging, 224(1), 22–27.CrossRefGoogle ScholarPubMed
Hasler, B. P., Mehl, M. R., Bootzin, R. R., & Vazire, S. (2008b). Preliminary evidence of diurnal rhythms in everyday behaviors associated with positive affect. Journal of Research in Personality, 42, 1537–1546.CrossRefGoogle Scholar
Hasler, B. P., Sitnick, S. L., Shaw, D. S., & Forbes, E. E. (2013). An altered neural response to reward may contribute to alcohol problems among late adolescents with an evening chronotype. Psychiatry Research: Neuroimaging, 214(3), 357–364.CrossRefGoogle ScholarPubMed
Horne, J. A. (1993). Human sleep, sleep loss and behaviour. Implications for the prefrontal cortex and psychiatric disorder. British Journal of Psychiatry, 162, 413–419.CrossRefGoogle ScholarPubMed
IBM Corp. (2017). IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY: IBM Corp.Google Scholar
Kang, J. I., Park, C. I., Sohn, S. Y., Kim, H. W., Namkoong, K., & Kim, S. J. (2015). Circadian preference and trait impulsivity, sensation-seeking and response inhibition in healthy young adults. Chronobiology International, 32(2), 235–241.CrossRefGoogle ScholarPubMed
Kaufman, J., Birmaher, B., Brent, D., Rao, U., & Ryan, N. (1996). Kiddie SADS– present and lifetime version (K–SADS–PL). Unpublished instrument. Pittsburgh, PA: Western Psychiatric Institute and Clinics, University of Pittsburgh School of Medicine.Google Scholar
Koenig, L. B., Jacob, T., & Haber, J. R. (2009). Validity of the lifetime drinking history: A comparison of retrospective and prospective quantity-frequency measures. Journal of Studies on Alcohol and Drugs, 70(2), 296–303.CrossRefGoogle ScholarPubMed
Kragel, P., Han, X., Kraynak, T., Gianaros, P. J., & Wager, T. (2020). fMRI can be highly reliable, but it depends on what you measure. https://doi.org/10.31234/osf.io/9eaxk.CrossRefGoogle Scholar
Landgraf, D., Long, J. E., Proulx, C. D., Barandas, R., Malinow, R., & Welsh, D. K. (2016a). Genetic disruption of circadian rhythms in the suprachiasmatic nucleus causes helplessness, behavioral despair, and anxiety-like behavior in mice. Biological Psychiatry, 80(11), 827–835.CrossRefGoogle ScholarPubMed
Landgraf, D., Long, J. E., & Welsh, D. K. (2016b). Depression-like behaviour in mice is associated with disrupted circadian rhythms in nucleus accumbens and periaqueductal grey. European Journal of Neuroscience, 43(10), 1309–1320.CrossRefGoogle ScholarPubMed
Logan, R. W., Hasler, B. P., Forbes, E. E., Franzen, P. L., Torregrossa, M. M., Huang, Y. H., … McClung, C. A. (2018). Impact of sleep and circadian rhythms on addiction vulnerability in adolescents. Biological Psychiatry, 83(12), 987–996.CrossRefGoogle ScholarPubMed
Luke, S. G. (2017). Evaluating significance in linear mixed-effects models in R. Behavior Research Methods, 49(4), 1494–1502.CrossRefGoogle ScholarPubMed
Minges, K. E., & Redeker, N. S. (2016). Delayed school start times and adolescent sleep: A systematic review of the experimental evidence. Sleep Medicine Reviews, 28, 86–95.CrossRefGoogle ScholarPubMed
Mongrain, V., Lavoie, S., Selmaoui, B., Paquet, J., & Dumont, M. (2004). Phase relationships between sleep-wake cycle and underlying circadian rhythms in morningness-eveningness. Journal of Biological Rhythms, 19(3), 248–257.CrossRefGoogle ScholarPubMed
Murray, G., Nicholas, C. L., Kleiman, J., Dwyer, R., Carrington, M. J., Allen, N. B., & Trinder, J. (2009). Nature's clocks and human mood: The circadian system modulates reward motivation. Emotion, 9(5), 705–716.CrossRefGoogle ScholarPubMed
Nilsson, J. P., Söderström, M., Karlsson, A. U., Lekander, M., Åkerstedt, T., Lindroth, N. E., & Axelsson, J. (2005). Less effective executive functioning after one night's sleep deprivation. Journal of Sleep Research, 14(1), 1–6.CrossRefGoogle ScholarPubMed
Norman, A. L., Pulido, C., Squeglia, L. M., Spadoni, A. D., Paulus, M. P., & Tapert, S. F. (2011). Neural activation during inhibition predicts initiation of substance use in adolescence. Drug and Alcohol Dependence, 119(3), 216–223.CrossRefGoogle ScholarPubMed
Paine, S. J., & Gander, P. H. (2016). Differences in circadian phase and weekday/weekend sleep patterns in a sample of middle-aged morning types and evening types. Chronobiology International, 33(8), 1009–1017.CrossRefGoogle Scholar
Parekh, P. K., & McClung, C. A. (2016). Circadian mechanisms underlying reward-related neurophysiology and synaptic plasticity. Frontiers in Psychiatry, 6, 187.CrossRefGoogle ScholarPubMed
Plichta, M. M., Schwarz, A. J., Grimm, O., Morgen, K., Mier, D., Haddad, L., … Meyer-Lindenberg, A. (2012). Test-retest reliability of evoked BOLD signals from a cognitive-emotive fMRI test battery. NeuroImage, 60(3), 1746–1758.CrossRefGoogle ScholarPubMed
Prendergast, B. J., Onishi, K. G., Patel, P. N., & Stevenson, T. J. (2014). Circadian arrhythmia dysregulates emotional behaviors in aged Siberian hamsters. Behavioural Brain Research, 261, 146–157.CrossRefGoogle ScholarPubMed
Roach, G. D., Dawson, D., & Lamond, N. (2006). Can a shorter psychomotor vigilance task be used as a reasonable substitute for the ten-minute psychomotor vigilance task? Chronobiology International, 23(6), 1379–1387.CrossRefGoogle ScholarPubMed
Russo, P. M., Leone, L., Penolazzi, B., & Natale, V. (2012). Circadian preference and the big five: The role of impulsivity and sensation seeking. Chronobiology International, 29(8), 1121–1126.CrossRefGoogle ScholarPubMed
Short, M. A., Weber, N., Reynolds, C., Coussens, S., & Carskadon, M. A. (2018). Estimating adolescent sleep need using dose-response modeling. Sleep, 41(4), zsy011.CrossRefGoogle ScholarPubMed
Soehner, A. M., Bertocci, M. A., Manelis, A., Bebko, G., Ladouceur, C. D., Graur, S., … Axelson, D. (2016). Preliminary investigation of the relationships between sleep duration, reward circuitry function, and mood dysregulation in youth offspring of parents with bipolar disorder. Journal of Affective Disorders, 205, 144–153.CrossRefGoogle ScholarPubMed
Song, J., Feng, P., Wu, X., Li, B., Su, Y., Liu, Y., & Zheng, Y. (2019). Individual differences in the neural basis of response inhibition after sleep deprivation are mediated by chronotype. Frontiers in Neurology, 10, 514.CrossRefGoogle ScholarPubMed
Song, J., Feng, P., Zhao, X., Xu, W., Xiao, L., Zhou, J., & Zheng, Y. (2018). Chronotype regulates the neural basis of response inhibition during the daytime. Chronobiology International, 35(2), 208–218.CrossRefGoogle ScholarPubMed
Swanson, L. M., Burgess, H. J., Huntley, E. D., Bertram, H., Mooney, A., Zollars, J., … Arnedt, J. T. (2017). Relationships between circadian measures, depression, and response to antidepressant treatment: A preliminary investigation. Psychiatry Research, 252, 262–269.CrossRefGoogle ScholarPubMed
Voultsios, A., Kennaway, D. J., & Dawson, D. (1997). Salivary melatonin as a circadian phase marker: Validation and comparison to plasma melatonin. Journal of Biological Rhythms, 12(5), 457–466.CrossRefGoogle ScholarPubMed
Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and validation of brief measures of positive affect and negative affect: The PANAS scales. Journal of Personality and Social Psychology, 54(6), 1063–1070.CrossRefGoogle ScholarPubMed
Wittmann, M., Dinich, J., Merrow, M., & Roenneberg, T. (2006). Social jetlag: Misalignment of biological and social time. Chronobiology International, 23(1&2), 497–509.CrossRefGoogle ScholarPubMed
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