Dataset Information

Non-sinusoidal Waveform in Temperature-Compensated Circadian Oscillations.

ABSTRACT: Time series of biological rhythms are of various shapes. Here, we investigated the waveforms of circadian rhythms in gene-protein dynamics using a newly developed, to our knowledge, index to quantify the degree of distortion from a sinusoidal waveform. In general, most biochemical reactions accelerate with increasing temperature, but the period of circadian rhythms remains relatively stable with temperature change, a phenomenon known as "temperature compensation." Despite extensive research, the mechanism underlying this remains unclear. To understand the mechanism, we used transcriptional-translational oscillator models for circadian rhythms in the fruit fly Drosophila and mammals. Given the assumption that reaction rates increase with temperature, mathematical analyses revealed that temperature compensation required waveforms that are more nonsinusoidal at higher temperatures. We then analyzed a post-translational oscillator (PTO) model of cyanobacteria circadian rhythms. Because the structure of the PTO is different from that of the transcriptional-translational oscillator, the condition for temperature compensation would be expected to differ. Unexpectedly, the computational analysis again showed that temperature compensation in the PTO model required a more nonsinusoidal waveform at higher temperatures. This finding held for both models even with a milder assumption that some reaction rates do not change with temperature, which is consistent with experimental evidence. Together, our theoretical analyses predict that the waveform of circadian gene-activity and/or protein phosphorylation rhythms would be more nonsinusoidal at higher temperatures, even when there are differences in the network structures.

SUBMITTER: Gibo S

PROVIDER: S-EPMC6383000 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Publications

Non-sinusoidal Waveform in Temperature-Compensated Circadian Oscillations.

Gibo Shingo S Kurosawa Gen G

Biophysical journal 20190115 4

Time series of biological rhythms are of various shapes. Here, we investigated the waveforms of circadian rhythms in gene-protein dynamics using a newly developed, to our knowledge, index to quantify the degree of distortion from a sinusoidal waveform. In general, most biochemical reactions accelerate with increasing temperature, but the period of circadian rhythms remains relatively stable with temperature change, a phenomenon known as "temperature compensation." Despite extensive research, the ...[more]

PMID: 30712786

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Project description:Neuronal oscillations support cognitive processing. Modern views suggest that neuronal oscillations do not only reflect coordinated activity in spatially distributed networks, but also that there is interaction between the oscillations at different frequencies. For example, invasive recordings in animals and humans have found that the amplitude of fast oscillations (>40 Hz) occur non-uniformly within the phase of slower oscillations, forming the so-called cross-frequency coupling (CFC). However, the CFC patterns might be influenced by features in the signal that do not relate to underlying physiological interactions. For example, CFC estimates may be sensitive to spectral correlations due to non-sinusoidal properties of the alpha band wave morphology. To investigate this issue, we performed CFC analysis using experimental and synthetic data. The former consisted in a double-blind magnetoencephalography pharmacological study in which participants received either placebo, 0.5 or 1.5 mg of lorazepam (LZP; GABAergic enhancer) in different experimental sessions. By recording oscillatory brain activity with during rest and working memory (WM), we were able to demonstrate that posterior alpha (8-12 Hz) phase was coupled to beta-low gamma band (20-45 Hz) amplitude envelope during all sessions. Importantly, bicoherence values around the harmonics of the alpha frequency were similar both in magnitude and topographic distribution to the cross-frequency coherence (CFCoh) values observed in the alpha-phase to beta-low gamma coupling. In addition, despite the large CFCoh we found no significant cross-frequency directionality (CFD). Critically, simulations demonstrated that a sizable part of our empirical CFCoh between alpha and beta-low gamma coupling and the lack of CFD could be explained by two-three harmonics aligned in zero phase-lag produced by the physiologically characteristic alpha asymmetry in the amplitude of the peaks relative to the troughs. Furthermore, we showed that periodic signals whose waveform deviate from pure sine waves produce non-zero CFCoh with predictable CFD. Our results reveal the important role of the non-sinusoidal wave morphology on state of the art CFC metrics and we recommend caution with strong physiological interpretations of CFC and suggest basic data quality checks to enhance the mechanistic understanding of CFC.

Dataset Information

Non-sinusoidal Waveform in Temperature-Compensated Circadian Oscillations.

Publications

Non-sinusoidal Waveform in Temperature-Compensated Circadian Oscillations.

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