Jessica R. Lunsford-Avery PhD , Mary A. Carskadon PhD , Scott H. Kollins PhD , Andrew D. Krystal MD
{"title":"Sleep Physiology and Neurocognition Among Adolescents With Attention-Deficit/Hyperactivity Disorder","authors":"Jessica R. Lunsford-Avery PhD , Mary A. Carskadon PhD , Scott H. Kollins PhD , Andrew D. Krystal MD","doi":"10.1016/j.jaac.2024.03.005","DOIUrl":null,"url":null,"abstract":"<div><h3>Objective</h3><div><span>Few studies have characterized the nature of sleep problems among adolescents with attention-deficit/hyperactivity disorder (ADHD) using polysomnography (PSG). Additionally, although adolescents with ADHD and adolescents with sleep disturbances display similar neurocognitive deficits, the role of sleep in contributing to neurocognitive impairment </span>in adolescent ADHD<span> is unknown. This study investigated differences in PSG-measured sleep among adolescents with ADHD compared with non-psychiatric controls and associations with neurocognition.</span></div></div><div><h3>Method</h3><div><span>Medication-free adolescents aged 13 to 17 (N = 62, n = 31 with ADHD; mean age = 15.3 years; 50% female) completed a diagnostic evaluation, 3 nights of ambulatory PSG, the Cambridge Neuropsychological Test Automated Battery, and subjective reports of sleep and executive functioning. </span>Linear regressions covarying for age, sex, and pubertal status examined group differences in sleep indices, and partial Pearson correlations assessed relations between sleep and neurocognition.</div></div><div><h3>Results</h3><div><span>Although adolescents with ADHD did not exhibit differences in PSG-measured sleep duration, awakenings, or latency (</span><em>p</em><span>s > .05) compared with non-psychiatric controls, they displayed lower slow wave sleep percentage (β = −.40) and non–rapid eye movement (NREM) electroencephalogram (EEG) delta power (β = −.29). They also exhibited greater stage 2 percentage (β = .41), NREM EEG sigma power (β = .41), and elevated self-reported sleep disturbances (</span><em>p</em>s < .05). Lower NREM EEG delta power, increased high-frequency power, and slower decline in NREM EEG delta power overnight were associated with poorer neurocognition among adolescents with ADHD.</div></div><div><h3>Conclusion</h3><div>Adolescents with ADHD reported more sleep disturbances than non-psychiatric controls and exhibited differences in sleep stage distribution and NREM sleep<span> EEG frequency. Sleep-EEG spectral indices were associated with impaired neurocognition, suggesting that physiological sleep processes may underlie neurocognitive deficits in ADHD. Future studies may clarify whether sleep plays a causal role in neurocognitive impairments in adolescent ADHD and whether interventions normalizing sleep improve neurocognition.</span></div></div><div><h3>Plain language summary</h3><div>This study investigated the sleep physiology in a sample of 62 adolescents, 31 with attention-deficit/hyperactivity disorder (ADHD) and 31 with no psychiatric diagnoses, aged 13 to 17. The authors found that medication-free adolescents with ADHD displayed reduced time in deep slow wave sleep, and increased time in lighter stage 2 sleep, than adolescents without a psychiatric diagnosis. Results indicate that disruptions in the amount and pattern of slow wave electroencephalogram (EEG) activity, as well as increased high frequency EEG power during sleep, were associated with lower cognitive performance among adolescents with ADHD. The study findings suggest that sleep physiology may contribute to cognitive deficits in ADHD and future research should assess whether interventions normalizing sleep improve cognitive performance in adolescents with ADHD.</div></div><div><h3>Clinical trial registration information</h3><div>Sleep Dysfunction and Neurocognitive Outcomes in Adolescent ADHD; <span><span>https://clinicaltrials.gov/</span><svg><path></path></svg></span>; NCT02897362.</div></div><div><h3>Diversity & Inclusion Statement</h3><div>We worked to ensure sex and gender balance in the recruitment of human participants. We worked to ensure race, ethnic, and/or other types of diversity in the recruitment of human participants. We worked to ensure that the study questionnaires were prepared in an inclusive way. One or more of the authors of this paper self-identifies as a member of one or more historically underrepresented sexual and/or gender groups in science. We actively worked to promote sex and gender balance in our author group. While citing references scientifically relevant for this work, we also actively worked to promote sex and gender balance in our reference list.</div></div>","PeriodicalId":17186,"journal":{"name":"Journal of the American Academy of Child and Adolescent Psychiatry","volume":"64 2","pages":"Pages 276-289"},"PeriodicalIF":9.2000,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of the American Academy of Child and Adolescent Psychiatry","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0890856724001230","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PEDIATRICS","Score":null,"Total":0}
引用次数: 0
Abstract
Objective
Few studies have characterized the nature of sleep problems among adolescents with attention-deficit/hyperactivity disorder (ADHD) using polysomnography (PSG). Additionally, although adolescents with ADHD and adolescents with sleep disturbances display similar neurocognitive deficits, the role of sleep in contributing to neurocognitive impairment in adolescent ADHD is unknown. This study investigated differences in PSG-measured sleep among adolescents with ADHD compared with non-psychiatric controls and associations with neurocognition.
Method
Medication-free adolescents aged 13 to 17 (N = 62, n = 31 with ADHD; mean age = 15.3 years; 50% female) completed a diagnostic evaluation, 3 nights of ambulatory PSG, the Cambridge Neuropsychological Test Automated Battery, and subjective reports of sleep and executive functioning. Linear regressions covarying for age, sex, and pubertal status examined group differences in sleep indices, and partial Pearson correlations assessed relations between sleep and neurocognition.
Results
Although adolescents with ADHD did not exhibit differences in PSG-measured sleep duration, awakenings, or latency (ps > .05) compared with non-psychiatric controls, they displayed lower slow wave sleep percentage (β = −.40) and non–rapid eye movement (NREM) electroencephalogram (EEG) delta power (β = −.29). They also exhibited greater stage 2 percentage (β = .41), NREM EEG sigma power (β = .41), and elevated self-reported sleep disturbances (ps < .05). Lower NREM EEG delta power, increased high-frequency power, and slower decline in NREM EEG delta power overnight were associated with poorer neurocognition among adolescents with ADHD.
Conclusion
Adolescents with ADHD reported more sleep disturbances than non-psychiatric controls and exhibited differences in sleep stage distribution and NREM sleep EEG frequency. Sleep-EEG spectral indices were associated with impaired neurocognition, suggesting that physiological sleep processes may underlie neurocognitive deficits in ADHD. Future studies may clarify whether sleep plays a causal role in neurocognitive impairments in adolescent ADHD and whether interventions normalizing sleep improve neurocognition.
Plain language summary
This study investigated the sleep physiology in a sample of 62 adolescents, 31 with attention-deficit/hyperactivity disorder (ADHD) and 31 with no psychiatric diagnoses, aged 13 to 17. The authors found that medication-free adolescents with ADHD displayed reduced time in deep slow wave sleep, and increased time in lighter stage 2 sleep, than adolescents without a psychiatric diagnosis. Results indicate that disruptions in the amount and pattern of slow wave electroencephalogram (EEG) activity, as well as increased high frequency EEG power during sleep, were associated with lower cognitive performance among adolescents with ADHD. The study findings suggest that sleep physiology may contribute to cognitive deficits in ADHD and future research should assess whether interventions normalizing sleep improve cognitive performance in adolescents with ADHD.
Clinical trial registration information
Sleep Dysfunction and Neurocognitive Outcomes in Adolescent ADHD; https://clinicaltrials.gov/; NCT02897362.
Diversity & Inclusion Statement
We worked to ensure sex and gender balance in the recruitment of human participants. We worked to ensure race, ethnic, and/or other types of diversity in the recruitment of human participants. We worked to ensure that the study questionnaires were prepared in an inclusive way. One or more of the authors of this paper self-identifies as a member of one or more historically underrepresented sexual and/or gender groups in science. We actively worked to promote sex and gender balance in our author group. While citing references scientifically relevant for this work, we also actively worked to promote sex and gender balance in our reference list.
期刊介绍:
The Journal of the American Academy of Child & Adolescent Psychiatry (JAACAP) is dedicated to advancing the field of child and adolescent psychiatry through the publication of original research and papers of theoretical, scientific, and clinical significance. Our primary focus is on the mental health of children, adolescents, and families.
We welcome unpublished manuscripts that explore various perspectives, ranging from genetic, epidemiological, neurobiological, and psychopathological research, to cognitive, behavioral, psychodynamic, and other psychotherapeutic investigations. We also encourage submissions that delve into parent-child, interpersonal, and family research, as well as clinical and empirical studies conducted in inpatient, outpatient, consultation-liaison, and school-based settings.
In addition to publishing research, we aim to promote the well-being of children and families by featuring scholarly papers on topics such as health policy, legislation, advocacy, culture, society, and service provision in relation to mental health.
At JAACAP, we strive to foster collaboration and dialogue among researchers, clinicians, and policy-makers in order to enhance our understanding and approach to child and adolescent mental health.