Circadian clock and attention deficit hyperactivity disorder

doi:10.11852/zgetbjzz2022-1546

Abstract

Abstract: The circadian clock produces a stable 24-hour circadian rhythm, which plays a crucial role in sleep, attention, learning, memory and cognition. Attention deficit hyperactivity disorder (ADHD) is one of the most common neurodevelopmental disorders in children. Circadian rhythm system dysfunction and sleep problems are found to be more common in ADHD compared to healthy children these years, which can worsen the symptoms of ADHD in turn. The circadian clock can regulate various physiological and biochemical processes related to ADHD, including hypothalamus-pituitary-adrenal axis, monoaminergic neurotransmitter system. This review will address the interaction between circadian system and processes above as well as their potential role in the development of ADHD.

Key words: circadian clock, circadian rhythms, attention deficit hyperactivity disorder, hypothalamus-pituitary-adrenal axis, monoaminergic neurotransmitter system

摘要： 生物钟产生稳定的24h昼夜节律,在机体睡眠、注意、学习、记忆、认知等生理过程中起着至关重要的作用。注意缺陷多动障碍(ADHD)是最常见的儿童神经发育障碍性疾病之一,近年来发现ADHD昼夜节律紊乱和睡眠问题较普遍,这又会反过来加重ADHD的症状。生物钟参与调节与ADHD密切相关的各种生理生化过程,其中包括下丘脑-垂体-肾上腺轴、单胺能系统。本综述将涉及生物钟和这些过程之间的相互作用,并讨论它们在ADHD发展中的潜在作用。

关键词: 生物钟, 昼夜节律, 注意缺陷多动障碍, 下丘脑-垂体-肾上腺轴, 单胺能系统

CLC Number:

R749.94

HUANG Huifang, CHEN Yanhui, HUANG Yuxian. Circadian clock and attention deficit hyperactivity disorder[J]. Chinese Journal of Child Health Care, 2023, 31(11): 1230-1234.

黄惠芳, 陈燕惠, 黄玉娴. 生物钟与注意缺陷多动障碍[J]. 中国儿童保健杂志, 2023, 31(11): 1230-1234.

References

[1] Meyer N, Harvey AG, Lockley SW,et al. Circadian rhythms and disorders of the timing of sleep[J]. Lancet,2022,400(10357):1061-1078.
[2] Salehinejad MA, Wischnewski M, Ghanavati E ,et al. Cognitive functions and underlying parameters of human brain physiology are associated with chronotype[J]. Nat Commun,2021,12(1):4672.
[3] Fagiani F, Di Marino D, Romagnoli A, et al. Molecular regulations of circadian rhythm and implications for physiology and diseases[J]. Signal Transduct Target Ther,2022,7(1):41.
[4] Guan D, Lazar MA. Interconnections between circadian clocks and metabolism[J]. J Clin Invest,2021,131(15):e148278.
[5] Mimouni-Bloch A, Offek H, Engel-Yeger B, et al. Association between sensory modulation and sleep difficulties in children withattention deficit hyperactivity disorder (ADHD)[J]. Sleep Med,2021,84:107-113.
[6] Bondopadhyay U, Diaz-Orueta U, Coogan AN. A Systematic review of sleep and circadian rhythms in children with attention deficit hyperactivity disorder[J]. J Atten Disord,2022,26(2):149-224.
[7] Costa R, Kyriacou C. Editorial: Entrainment of biological rhythms[J]. Front Physiol,2021,12:757000.
[8] Yuan Y, Xiao Y, Yadlapalli S. The role of spatiotemporal organization and dynamics of clock complexes in circadian regulation[J]. Curr Opin Cell Biol,2022,78:102129.
[9] Boyce WT, Sokolowski MB, Robinson GE. Genes and environments, development and time[J]. Proc Natl Acad Sci U S A,2020,117(38):23235-23241.
[10] Reh RK, Dias BG, Nelson CA, et al. Critical period regulation across multiple timescales[J]. Proc Natl Acad Sci U S A,2020,117(38):23242-23251.
[11] Nicolaides NC, Kyratzi E, Lamprokostopoulou A, et al. Stress, the stress system and the role of glucocorticoids[J]. Neuroimmunomodulation,2015,22(1-2):6-19.
[12] Molins F, Serrano MÁ, Alacreu-Crespo A. Early stages of the acute physical stress response increase loss aversion and learning on decision making: A Bayesian approach[J]. Physiol Behav,2021,237:113459.
[13] Zerbes G, Kausche FM, Schwabe L. Stress-induced cortisol modulates the control of memory retrieval towards the dorsal striatum[J]. Eur J Neurosci,2022,55(9-10):2699-2713.
[14] Angeli E, Korpa T, Johnson EO, et al. Salivary cortisol and alpha-amylase diurnal profiles and stress reactivity in children with attention deficit hyperactivity disorder[J].Psychoneuroendocrinology,2018,90:174-181.
[15] Buske-Kirschbaum A, Trikojat K, Tesch F, et al. Altered hypothalamus-pituitary-adrenal axis function: A relevant factor in the comorbidity of atopic eczema and attention deficit/hyperactivity disorder?[J].Psychoneuroendocrinology,2019, 105:178-186.
[16] Ma L, Chen YH, Chen H,et al. The function of hypothalamus-pituitary-adrenal axis in children with ADHD[J].Brain Res,2011,1368:159-162.
[17] Northover C, Thapar A, Langley K,et al. Cortisol levels at baseline an under stress in adolescent males with attention-deficit hyperactivity disorder, with or without comorbid conduct disorder[J].Psychiatry Res,2016,242:130-136.
[18] 陈辉. 注意缺陷多动障碍HPA轴功能的临床及实验研究[D].福州:福建医科大学,2010.
Chen H. Clinical and experimental studies of HPA axis function in attention deficit hyperactivity disorder[D]. Fuzhou: Fujian Medical University, 2010. (in Chinese)
[19] Baird AL, Coogan AN, Siddiqui A, et al. Adult attention-deficit hyperactivity disorder is associated with alterations in circadian rhythms at the behavioural, endocrine and molecular levels[J]. Mol Psychiatry,2012,17(10):988-995.
[20] Focke CMB, Iremonger KJ. Rhythmicity matters: Circadian and ultradian patterns of HPA axis activity[J]. Mol Cell Endocrinol,2020,501:110652.
[21] Spencer RL, Chun LE, Hartsock MJ, et al. Glucocorticoid hormones are both a major circadian signal and major stress signal: How this shared signal contributes to a dynamic relationship between the circadian and stress systems[J]. Front Neuroendocrinol,2018,49:52-71.
[22] Russell AL, Miller L, Yi H, et al. Knockout of the circadian gene, Per2, disrupts corticosterone secretion and results in depressive-like behaviors and deficits in startle responses[J]. BMC Neurosci,2021,22(1):5.
[23] Lamia KA, Papp SJ, Yu RT, et al. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor[J]. Nature,2011,480(7378):552-556.
[24] Han DH, Lee YJ, Kim K, et al. Modulation of glucocorticoid receptor induction properties by core circadian clock proteins[J]. Mol Cell Endocrinol,2014,383(1-2):170-180.
[25] Spencer RL, Chun LE, Hartsock MJ, et al. Glucocorticoid hormones are both a major circadian signal and major stress signal: How this shared signal contributes to a dynamic relationship between the circadian and stress systems[J]. Front Neuroendocrinol,2018,49:52-71.
[26] Ionadi A, Johnson JD. Interaction between corticosterone and PER2 in regulating emotional behaviors in the rat[J]. Psychoneuroendocrinology,2022,137:105628.
[27] Sakurada K, Konta T, Takahashi S, et al. Circadian clock gene polymorphisms and sleep-onset problems in a population-based cohort study: The yamagata study[J]. Tohoku J Exp Med,2021,255(4):325-331.
[28] Choshen-Hillel S, Ishqer A, Mahameed F, et al. Acute and chronic sleep deprivation in residents: Cognition and stress biomarkers[J]. Med Educ,2021,55(2):174-184.
[29] Rao R, Somvanshi P, Klerman EB, et al. Modeling the influence of chronic sleep restriction on cortisol circadian rhythms, with implications for metabolic disorders[J]. Metabolites,2021,11(8):483.
[30] Ehichioya DE, Tahajjul Taufique SK, Anigbogu CN, et al. Effect of rapid eye movement sleep deprivation during pregnancy on glucocorticoid receptor regulation of HPA axis function in female offspring[J]. Brain Res,2022,1781:147823.
[31] Raftopoulou S, Nicolaides NC, Papageorgiou L, et al. Structural study of the DNA: Clock/Bmal1 complex provides insights for the role of cortisol, hGR, and HPA axis in stress management and sleep disorders[J]. Adv Exp Med Biol, 2020,1195:59-71.
[32] Zhang L, McCarthy DM, Eskow Jaunarajs KL, et al. Frontal cortical monoamine release, attention, and working memory in a perinatal nicotine exposure mouse model following kappa opioid receptor antagonism[J].Cereb Cortex,2021,31(1):483-496.
[33] Barkley RA, Smith KM, Fischer M. ADHD risk genes involved in dopamine signaling and metabolism are associated with reduced estimated life expectancy at young adult follow-up in hyperactive and control children[J]. Am J Med Genet B Neuropsychiatr Genet,2019,180(3):175-185.
[34] Nikolaus S, Mamlins E, Giesel FL, et al. Monoaminergic hypo - or hyperfunction in adolescent and adult attention-deficit hyperactivity disorder?[J]. Rev Neurosci,2021,33(4):347-364.
[35] Riley TB, Overton PG. Enhancing the efficacy of 5-HT uptake inhibitors in the treatment of attention deficit hyperactivity disorder[J]. Med Hypotheses, 2019,133:109407.
[36] Di Miceli M, Derf A, Gronier B. Consequences of acute or chronic methylphenidate exposure using ex vivo neurochemistry and in vivo electrophysiology in the prefrontal cortex and striatum of rats[J]. Int J Mol Sci,2022,23(15):8588.
[37] Aster HC, Romanos M, Walitza S, et al. Responsivity of the striatal dopamine system to methylphenidate-A within-subject I-123-β-CIT-SPECT study in male children and adolescents with attention-deficit/hyperactivity disorder[J]. Front Psychiatry,2022,13:804730.
[38] Rosenau PT, Openneer TJC, Matthijssen AM, et al. Effects of methylphenidate on executive functioning in children and adolescents with ADHD after long-term use: A randomized, placebo-controlled discontinuation study[J]. J Child Psychol Psychiatry,2021,62(12):1444-1452.
[39] Kim R, Witelski TP. Uncovering the dynamics of a circadian-dopamine model influenced by the light-dark cycle[J]. Math Biosci,2022,344:108764.
[40] Leach S, Suzuki K. Adrenergic signaling in circadian control of immunity[J]. Front Immunol,2020,11:1235.
[41] Weber M, Lauterburg T, Tobler I,et al. Circadian patterns of neurotransmitter related gene expression in motor regions of the rat brain[J]. Neurosci Lett,2004,358(1):17-20.
[42] Huang J, Zhong Z, Wang M, et al. Circadian modulation of dopamine levels and dopaminergic neuron development contributes to attention deficiency and hyperactive behavior[J]. J Neurosci,2015,35(6):2572-2587.
[43] Otsuka T, Le HT, Thein ZL, et al. Deficiency of the circadian clock gene Rev-erbα induces mood disorder-like behaviours and dysregulation of the serotonergic system in mice[J]. Physiol Behav. 2022,256:113960.
[44] Eban-Rothschild A, Appelbaum L, de Lecea L. Neuronal mechanisms for sleep/wake regulation and modulatory drive[J]. Neuropsychopharmacology,2018,43(5):937-952.
[45] Faltraco F, Palm D, Uzoni A, et al. Dopamine adjusts the circadian gene expression of Per2 and Per3 in human dermal fibroblasts from ADHD patients[J]. J Neural Transm (Vienna),2021,128(7):1135-1145.
[46] Palm D, Uzoni A, Simon F, et al. Norepinephrine influences the circadian clock in human dermal fibroblasts from study participants with a diagnosis of attention-deficit hyperactivity disorder[J]. J Neural Transm (Vienna),2021,128(7):1147-1157.
[47] Alghamdi BS. The neuroprotective role of melatonin in neurological disorders[J]. J Neurosci Res,2018,96(7):1136-1149.
[48] Lee BH, Hille B, Koh DS. Serotonin modulates melatonin synthesis as an autocrine neurotransmitter in the pineal gland[J]. Proc Natl Acad Sci USA, 2021,118(43):e2113852118.
[49] Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: A review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters[J]. Pharmacol Rev, 2003,55(2):325-395.
[50] Cenit MC, Nuevo IC, Codoñer-Franch P, et al. Gut microbiota and attention deficit hyperactivity disorder: New perspectives for a challenging condition[J]. Eur Child Adolesc Psychiatry, 2017,26(9):1081-1092.
[51] Prehn-Kristensen A, Zimmermann A, Tittmann L, et al. Reduced microbiome alpha diversity in young patients with ADHD[J]. PLoS One, 2018,13(7):e0200728.
[52] Heddes M, Altaha B, Niu Y, et al. The intestinal clock drives the microbiome to maintain gastrointestinal homeostasis[J]. Nat Commun, 2022,13(1):6068.
[53] Zhen Y, Ge L, Xu Q, et al. Normal light-dark and short-light cycles regulate intestinal inflammation, circulating short-chain fatty acids and gut microbiota in period2 gene knockout mice[J]. Front Immunol, 2022,13:848248.
[54] Ku K, Park I, Kim D, et al. Gut microbial metabolites induce changes in circadian oscillation of clock gene expression in the mouse embryonic fibroblasts[J]. Mol Cells, 2020,43(3):276-285.
[55] Desmet L, Thijs T, Segers A, et al. Chronodisruption by chronicjetlag impacts metabolic and gastrointestinal homeostasis in male mice[J]. Acta Physiol (Oxf), 2021,233(4):e13703.
[56] Becker SP. ADHD and sleep: Recent advances and future directions[J]. Curr Opin Psychol, 2020,34:50-56.
[57] Carpena MX, Hutz MH, Salatino-Oliveira A, et al. CLOCK polymorphisms in attention-deficit/hyperactivity disorder (ADHD): Further evidence linking sleep and circadian disturbances and ADHD[J]. Genes (Basel), 2019,10(2):88.
[58] Onat OE, Kars ME, Gül Ş, et al. Human CRY1 variants associate with attention deficit/hyperactivity disorder[J]. J Clin Invest, 2020,130(7):3885-3900.
[59] Wang Y, Peng S, Liu T, et al. The potential role of clock genes in children attention-deficit/hyperactivity disorder[J]. Sleep Med, 2020,71:18-27.
[60] Dück A, Reis O, Wagner H, et al. Clock genes profiles as diagnostic tool in (childhood) ADHD-A pilot study[J]. Brain Sci, 2022,12(9):1198.
[61] Korman M, Palm D, Uzoni A, et al. ADHD 24/7: Circadian clock genes, chronotherapy and sleep/wake cycle insufficiencies in ADHD[J]. World J Biol Psychiatry, 2020,21(3):156-171.
[62] Van Andel E, Bijlenga D, Vogel SWN, et al. Effects of chronotherapy on circadian rhythm and ADHD symptoms in adults with attention-deficit/hyperactivity disorder and delayed sleep phase syndrome: A randomized clinical trial[J]. Chronobiol Int, 2021,38(2):260-269.
[63] Rzepka-Migut B, Paprocka J. Efficacy and safety of melatonin treatment in children with autism spectrum disorder and attention-deficit/hyperactivity disorder-a review of the literature[J]. Brain Sci, 2020,10(4):219.
[64] Masi G, Fantozzi P, Villafranca A, et al. Effects of melatonin in children with attention-deficit/hyperactivity disorder with sleep disorders after methylphenidate treatment[J]. Neuropsychiatr Dis Treat, 2019,15:663-667.