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Simulated shift work in rats perturbs multiscale regulation of locomotor activity.

ABSTRACT: Motor activity possesses a multiscale regulation that is characterized by fractal activity fluctuations with similar structure across a wide range of timescales spanning minutes to hours. Fractal activity patterns are disturbed in animals after ablating the master circadian pacemaker (suprachiasmatic nucleus, SCN) and in humans with SCN dysfunction as occurs with aging and in dementia, suggesting the crucial role of the circadian system in the multiscale activity regulation. We hypothesized that the normal synchronization between behavioural cycles and the SCN-generated circadian rhythms is required for multiscale activity regulation. To test the hypothesis, we studied activity fluctuations of rats in a simulated shift work protocol that was designed to force animals to be active during the habitual resting phase of the circadian/daily cycle. We found that these animals had gradually decreased mean activity level and reduced 24-h activity rhythm amplitude, indicating disturbed circadian and behavioural cycles. Moreover, these animals had disrupted fractal activity patterns as characterized by more random activity fluctuations at multiple timescales from 4 to 12 h. Intriguingly, these activity disturbances exacerbated when the shift work schedule lasted longer and persisted even in the normal days (without forced activity) following the shift work. The disrupted circadian and fractal patterns resemble those of SCN-lesioned animals and of human patients with dementia, suggesting a detrimental impact of shift work on multiscale activity regulation.

SUBMITTER: Hsieh WH

PROVIDER: S-EPMC4032547 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Simulated shift work in rats perturbs multiscale regulation of locomotor activity.

Hsieh Wan-Hsin WH Escobar Carolina C Yugay Tatiana T Lo Men-Tzung MT Pittman-Polletta Benjamin B Salgado-Delgado Roberto R Scheer Frank A J L FA Scheer Frank A J L FA Shea Steven A SA Buijs Ruud M RM Hu Kun K

Journal of the Royal Society, Interface 20140701 96

Motor activity possesses a multiscale regulation that is characterized by fractal activity fluctuations with similar structure across a wide range of timescales spanning minutes to hours. Fractal activity patterns are disturbed in animals after ablating the master circadian pacemaker (suprachiasmatic nucleus, SCN) and in humans with SCN dysfunction as occurs with aging and in dementia, suggesting the crucial role of the circadian system in the multiscale activity regulation. We hypothesized that ...[more]

PMID: 24829282

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Project description:OBJECTIVE:Changes in heart rate (HR) and locomotor activity reflect changes in autonomic physiology, behavior, and mood. These systems may involve interrelated neural circuits that are altered in psychiatric illness, yet their interactions are poorly understood. We hypothesized interactions between HR and locomotor activity could be used to discriminate patients with schizophrenia from controls, and would be less able to discriminate non-psychiatric patients from controls. APPROACH:HR and locomotor activity were recorded via wearable patches in 16 patients with schizophrenia and 19 healthy controls. Measures of signal complexity and interactions were calculated over multiple time scales, including sample entropy, mutual information, and transfer entropy. A support vector machine was trained on these features to discriminate patients from controls. Additionally, time series were converted into a network with nodes comprised of HR and locomotor activity states, and edges representing state transitions. Graph properties were used as features. Leave-one-out cross validation was performed. To compare against non-psychiatric illness, the same approach was repeated in 41 patients with atrial fibrillation (AFib) and 53 controls. MAIN RESULTS:Network features enabled perfect discrimination of schizophrenia patients from controls with an areas under the receiver operating characteristic curve (AUC) of 1.00 for training and test data. Other bivariate measures of interaction achieved lower AUCs (train 0.98, test 0.96), and univariate measures of complexity achieved the lowest performance. Conversely, interaction features did not improve discrimination of AFib patients from controls beyond univariate approaches. SIGNIFICANCE:Interactions between HR and locomotor activity enabled perfect discrimination of subjects with schizophrenia from controls, but these features were less performant in a non-psychiatric illness. This is the first quantitative evaluation of interactions between physiology and behavior in patients with psychiatric illness.

Project description:Millions of people worldwide work during the night, resulting in disturbed circadian rhythms and sleep loss. This may cause deficits in cognitive functions, impaired alertness and increased risk of errors and accidents. Disturbed circadian rhythmicity resulting from night shift work could impair brain function and cognition through disrupted synthesis of proteins involved in synaptic plasticity and neuronal function. Recently, the circadian transcription factor brain-and-muscle arnt-like protein 1 (BMAL1) has been identified as a promoter of mRNA translation initiation, the most highly regulated step in protein synthesis, through binding to the mRNA "cap". In this study we investigated the effects of simulated shift work on protein synthesis markers. Male rats (n = 40) were exposed to forced activity, either in their rest phase (simulated night shift work) or in their active phase (simulated day shift work) for 3 days. Following the third work shift, experimental animals and time-matched undisturbed controls were euthanized (rest work at ZT12; active work at ZT0). Tissue lysates from two brain regions (prefrontal cortex, PFC and hippocampus) implicated in cognition and sleep loss, were analyzed with m7GTP (cap) pull-down to examine time-of-day variation and effects of simulated shift work on cap-bound protein translation. The results show time-of-day variation of protein synthesis markers in PFC, with increased protein synthesis at ZT12. In the hippocampus there was little difference between ZT0 and ZT12. Active phase work did not induce statistically significant changes in protein synthesis markers at ZT0 compared to time-matched undisturbed controls. Rest work, however, resulted in distinct brain-region specific changes of protein synthesis markers compared to time-matched controls at ZT12. While no changes were observed in the hippocampus, phosphorylation of cap-bound BMAL1 and its regulator S6 kinase beta-1 (S6K1) was significantly reduced in the PFC, together with significant reduction in the synaptic plasticity associated protein activity-regulatedcytoskeleton-associated protein (Arc). Our results indicate considerable time-of-day and brain-region specific variation in cap-dependent translation initiation. We concludethat simulated night shift work in rats disrupts the pathways regulating the circadian component of the translation of mRNA in the PFC, and that this may partly explain impaired waking function during night shift work.

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Simulated shift work in rats perturbs multiscale regulation of locomotor activity.

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Simulated shift work in rats perturbs multiscale regulation of locomotor activity.

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