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Childhood high-frequency EEG activity during sleep is associated with incident insomnia symptoms in adolescence.

ABSTRACT: BACKGROUND:Insomnia has been associated in cross-sectional studies with increased beta (15-35 Hz) electroencephalogram (EEG) power during nonrapid eye movement (NREM) sleep, an index of cortical hyperarousal. However, it is unknown whether this cortical hyperarousal is present before individuals with insomnia develop the disorder. To fill this gap, we examined the association of childhood sleep high-frequency EEG activity with incident insomnia symptoms (i.e., absence of insomnia symptoms in childhood but presence in adolescence). METHODS:We studied a case-control subsample of 45 children (6-11 years) from the Penn State Child Cohort, a population-based random sample of 421 children, who were followed up after 8 years as adolescents (13-20 years). We examined low-beta (15-25 Hz) and high-beta (25-35 Hz) relative power at central EEG derivations during NREM sleep and, in secondary analyses, during sleep onset latency, sleep onset, and REM sleep. Incident insomnia symptoms were defined as the absence of parent-reported difficulty falling and/or staying asleep during childhood and a self-report of these insomnia symptoms during adolescence. RESULTS:Childhood high-beta power during NREM sleep was significantly increased in children who developed insomnia symptoms in adolescence (n = 25) as compared to normal sleeping controls (n = 20; p = .03). Multivariable-adjusted logistic regression models showed that increased childhood high-beta EEG power during NREM sleep was associated with a threefold increased odds (95% CI = 1.12-7.98) of incident insomnia symptoms in adolescence. No other significant relationships were observed for other sleep/wake states or EEG frequency bands. CONCLUSIONS:Increased childhood high-frequency EEG power during NREM sleep is associated with incident insomnia symptoms in adolescence. This study indicates that cortical hyperarousal during sleep may be a premorbid neurophysiological sign of insomnia, which may mediate the increased risk of psychiatric disorders associated with insomnia.

SUBMITTER: Fernandez-Mendoza J

PROVIDER: S-EPMC6328336 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Childhood high-frequency EEG activity during sleep is associated with incident insomnia symptoms in adolescence.

Fernandez-Mendoza Julio J Li Yun Y Fang Jidong J Calhoun Susan L SL Vgontzas Alexandros N AN Liao Duanping D Bixler Edward O EO

Journal of child psychology and psychiatry, and allied disciplines 20180710 7

<h4>Background</h4>Insomnia has been associated in cross-sectional studies with increased beta (15-35 Hz) electroencephalogram (EEG) power during nonrapid eye movement (NREM) sleep, an index of cortical hyperarousal. However, it is unknown whether this cortical hyperarousal is present before individuals with insomnia develop the disorder. To fill this gap, we examined the association of childhood sleep high-frequency EEG activity with incident insomnia symptoms (i.e., absence of insomnia symptom ...[more]

PMID: 29989664

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Project description:ObjectiveThe study aims to evaluate the association between exposure to childhood adversity and insomnia, with an emphasis on the role of adversity type, timing, and accumulation (i.e., the number of specific types of adversities the child reported being exposed to).MethodsOur analytic sample comprised 9582 adolescents from the National Comorbidity Survey Replication Adolescent Supplement (NCS-A), a nationally representative population-based sample. We examined the association between 18 different types of retrospectively reported adversities (capturing interpersonal violence, accidents and injuries, social network or witnessing events, and other adverse events) and risk of self-reported past-year insomnia. We also examined whether the age at first exposure to adversity was associated with the risk of insomnia, and whether exposure to a greater number of different types of adversities (ie, accumulation) conferred an elevated risk of insomnia. In addition, we performed a sensitivity analysis excluding adolescents with a past-year diagnosis of major depression, dysthymia, post-traumatic stress disorder (PTSD), or generalized anxiety disorder.ResultsAlmost one-third of adolescents reported insomnia, with a higher prevalence among girls and those from racial/ethnic minority groups. Adolescents exposed to at least one childhood adversity of any type (59.41%) were more likely than their nonexposed peers to experience insomnia (across adversities, prevalence ratios (PRs) ranged from 1.31 to 1.89). Risk of insomnia differed based on the age at first exposure to adversity as well as the type of adversity. Adolescents exposed to a greater number of different types of adversities had a higher risk of insomnia compared to those experiencing fewer adversities. These results were similar, by and large, to those obtained after excluding adolescents with at least one of the four past-year psychiatric disorders.ConclusionsExposure to adversity confers an elevated risk of insomnia. This association varied by type, timing, and accumulation of exposure and did not appear to be driven by psychiatric disorders. Given the well-documented physical and mental health consequences of insomnia, such findings further support the need for practitioners to screen children for exposure to childhood adversity and insomnia symptoms.

Project description:Sleep disorders, such as insomnia and nightmares, are commonly associated with Borderline Personality Disorder (BPD) in adulthood. Whether nightmares and sleep-onset and maintenance problems predate BPD symptoms earlier in development is unknown. We addressed this gap in the literature using data from the Avon Longitudinal Study of Parents and Children (ALSPAC). Participants included 6050 adolescents (51.4 % female) who completed the UK Childhood Interview for DSM-IV BPD at 11 to 12 years of age. Nightmares and sleep onset and maintenance problems were prospectively assessed via mother report when children were 2.5, 3.5, 4.8 and 6.8 years of age. Psychopathological (i.e., emotional temperament; psychiatric diagnoses; and emotional and behavioural problems) and psychosocial (i.e., abuse, maladaptive parenting, and family adversity) confounders were assessed via mother report. In logistic regressions, persistent nightmares (i.e., regular nightmares at 3 or more time-points) were significantly associated with BPD symptoms following adjustment for sleep onset and maintenance problems and all confounders (Adjusted Odds Ratio = 1.62; 95 % Confidence Interval = 1.12 to 2.32). Persistent sleep onset and maintenance problems were not significantly associated with BPD symptoms. In path analysis controlling for all associations between confounders, persistent nightmares independently predicted BPD symptoms (Probit co-efficient [β] = 0.08, p = 0.013). Emotional and behavioural problems significantly mediated the association between nightmares and BPD (β =0.016, p < 0.001), while nightmares significantly mediated associations between emotional temperament (β = 0.001, p = 0.018), abuse (β = 0.015, p = 0.018), maladaptive parenting (β = 0.002, p = 0.021) and subsequent BPD. These findings tentatively support that childhood nightmares may potentially increase the risk of BPD symptoms in early adolescence via a number of aetiological pathways. If replicated, the current findings could have important implications for early intervention, and assist clinicians in the identification of children at risk of developing BPD.

Project description:High-frequency oscillations are markers of epileptic tissue. Recently, different patterns of EEG background activity were described from which high-frequency oscillations occur: high-frequency oscillations with continuously oscillating background were found to be primarily physiological, those from quiet background were linked to epileptic tissue. It is unclear, whether these interactions remain stable over several days and during different sleep-wake stages. High-frequency oscillation patterns (oscillatory vs. quiet background) were analysed in 23 patients implanted with depth and subdural grid electrodes. Pattern scoring was performed on every channel in 10 s intervals in three separate day- and night-time EEG segments. An entropy value, measuring variability of patterns per channel, was calculated. A low entropy value indicated a stable occurrence of the same pattern in one channel, whereas a high value indicated pattern instability. Differences in pattern distribution and entropy were analysed for 143 280 10 s intervals with allocated patterns from inside and outside the seizure onset zone, different electrode types and brain regions. We found a strong association between high-frequency oscillations out of quiet background activity, and channels of the seizure onset zone (35.2% inside versus 9.7% outside the seizure onset zone, P < 0.001), no association was found for high-frequency oscillations from continuous oscillatory background (P = 0.563). The type of background activity remained stable over the same brain region over several days and was independent of sleep stage and recording technique. Stability of background activity was significantly higher in channels of the seizure onset zone (entropy mean value 0.56 ± 0.39 versus 0.64 ± 0.41; P < 0.001). This was especially true for the presumed epileptic high-frequency oscillations out of quiet background (0.57 ± 0.39 inside versus 0.72 ± 0.37 outside the seizure onset zone; P < 0.001). In contrast, presumed physiological high-frequency oscillations from continuous oscillatory backgrounds were significantly more stable outside the seizure onset zone (0.72 ± 0.45 versus 0.48 ± 0.53; P < 0.001). The overall low entropy values suggest that interactions between high-frequency oscillations and background activity are a stable phenomenon specific to the function of brain regions. High-frequency oscillations occurring from a quiet background are strongly linked to the seizure onset zone whereas high-frequency oscillations from an oscillatory background are not. Pattern stability suggests distinct underlying mechanisms. Analysing short time segments of high-frequency oscillations and background activity could help distinguishing epileptic from physiologically active brain regions.

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Childhood high-frequency EEG activity during sleep is associated with incident insomnia symptoms in adolescence.

Publications

Childhood high-frequency EEG activity during sleep is associated with incident insomnia symptoms in adolescence.

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