A highly tunable dopaminergic oscillator generates ultradian rhythms of behavioral arousal

Blum, Ian D.; Zhu, Lei; Moquin, Luc; Kokoeva, Maia V.; Gratton, Alain; Giros, Bruno; Storch, Kai‐Florian

doi:10.7554/elife.05105

Cited by 145 publications

(208 citation statements)

References 83 publications

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“…Alternatively, this could be related to the decrease in DA, observed only for LO fish. Indeed it has recently been shown that a decrease in DA in mouse brain led to a shortening of ultradian activity period (higher fractionation of activity, [44]). Our results are also in agreement with behavioural changes observed in adult zebrafish after seven months of exposure to low BaP concentrations (waterborne exposure; effects seen starting at 0.05–0.5 nM (12.6–126 ng·L −1 )).…”

Section: Resultsmentioning

confidence: 99%

Changes in Brain Monoamines Underlie Behavioural Disruptions after Zebrafish Diet Exposure to Polycyclic Aromatic Hydrocarbons Environmental Mixtures

Vignet

Trenkel

Vouillarmet

et al. 2017

IJMS

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Zebrafish were exposed through diet to two environmentally relevant polycyclic aromatic hydrocarbons (PAHs) mixtures of contrasted compositions, one of pyrolytic (PY) origin and one from light crude oil (LO). Monoamine concentrations were quantified in the brains of the fish after six month of exposure. A significant decrease in noradrenaline (NA) was observed in fish exposed to both mixtures, while a decrease in serotonin (5HT) and dopamine (DA) was observed only in LO-exposed fish. A decrease in metabolites of 5HT and DA was observed in fish exposed to both mixtures. Several behavioural disruptions were observed that depended on mixtures, and parallels were made with changes in monoamine concentrations. Indeed, we observed an increase in anxiety in fish exposed to both mixtures, which could be related to the decrease in 5HT and/or NA, while disruptions of daily activity rhythms were observed in LO fish, which could be related to the decrease in DA. Taken together, these results showed that (i) chronic exposures to PAHs mixtures disrupted brain monoamine contents, which could underlie behavioural disruptions, and that (ii) the biological responses depended on mixture compositions.

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Section: Resultsmentioning

confidence: 99%

Changes in Brain Monoamines Underlie Behavioural Disruptions after Zebrafish Diet Exposure to Polycyclic Aromatic Hydrocarbons Environmental Mixtures

Vignet

Trenkel

Vouillarmet

et al. 2017

IJMS

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“…Independent of the SCN and of circadian clock function, chronic methamphetamine administration induces activity rhythms with a period close to 24 h (Mohawk et al, 2009;Tataroglu et al, 2006). A recent study from Blum and colleagues indicates that the MASCO is a manifestation of a newly discovered dopaminergic oscillator (Blum et al, 2014). They have shown that in the absence of a functional molecular circadian clock, hyperdopaminergic DAT À/ À mice have longer period ultradian rhythms, and increasing DA signaling can even evoke behavioral rhythms with periods up to 24 h and longer.…”

Section: Discussionmentioning

confidence: 99%

The mood stabilizer valproic acid opposes the effects of dopamine on circadian rhythms

et al. 2016

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a b s t r a c tEndogenous circadian (~24 h) clocks regulate key physiological and cognitive processes via rhythmic expression of clock genes. The main circadian pacemaker is the hypothalamic suprachiasmatic nucleus (SCN). Mood disorders, including bipolar disorder (BD), are commonly associated with disturbed circadian rhythms. Dopamine (DA) contributes to mania in BD and has direct impact on clock gene expression. Therefore, we hypothesized that high levels of DA during episodes of mania contribute to disturbed circadian rhythms in BD. The mood stabilizer valproic acid (VPA) also affects circadian rhythms. Thus, we further hypothesized that VPA normalizes circadian disturbances caused by elevated levels of DA. To test these hypotheses, we examined locomotor rhythms and circadian gene cycling in mice with reduced expression of the dopamine transporter (DAT-KD mice), which results in elevated DA levels and manialike behavior. We found that elevated DA signaling lengthened the circadian period of behavioral rhythms in DAT-KD mice and clock gene expression rhythms in SCN explants. In contrast, we found that VPA shortened circadian period of behavioral rhythms in DAT-KD mice and clock gene expression rhythms in SCN explants, hippocampal cell lines, and human fibroblasts from BD patients. Thus, DA and VPA have opposing effects on circadian period. To test whether the impact of VPA on circadian rhythms contributes to its behavioral effects, we fed VPA to DAT-deficient Drosophila with and without functioning circadian clocks. Consistent with our hypothesis, we found that VPA had potent activity-suppressing effects in hyperactive DAT-deficient flies with intact circadian clocks. However, these effects were attenuated in DAT-deficient flies in which circadian clocks were disrupted, suggesting that VPA functions partly through the circadian clock to suppress activity. Here, we provide in vivo and in vitro evidence across species that elevated DA signaling lengthens the circadian period, an effect remediated by VPA treatment. Hence, VPA may exert beneficial effects on mood by normalizing lengthened circadian rhythm period in subjects with elevated DA resulting from reduced DAT.

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“…Of note is that this seasonally responsive central thermostat governs the sensitivity of certain brain dopamine-2 (D 2 ) receptors [74], which are the therapeutic mood-stabilizing neuroreceptor targets for the atypical antipsychotic medications that are effective for mixed depressive states [17]. Further, genetic variations affecting central D 2 receptor function regulate variations in habitual sleep duration in humans [75], while striatal extracellular dopamine concentrations and striatal D 2 receptors modulate the activity-rest ratio in mice [76]. Thus, studies of the thermostat’s regulation of central D 2 receptors, dopamine, mood, arousal, and E-M and sleep duration in spring mixed depressive states become of interest [77].…”

Section: Discussionmentioning

confidence: 99%

Chris Cornell, the Black Hole Sun, and the Seasonality of Suicide

Schwartz¹

2019

Neuropsychobiology

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Purpose: Seattle-inspired rock and roll superstar Chris Cornell died by suicide in May 2017. In the northern hemisphere, May represents the peak of the widely replicated but still unexplained seasonal spring rhythm in suicide. Years earlier, Cornell had suffered openly from recurrent bouts of severe depression, and his early musical lyrics do indeed suggest an enduring sensitivity to the vicissitudes of depressed and suicidal states. Cornell’s most famous song, Black Hole Sun, suggests a mixed mood state, the incidence of which also peaks in the spring. The present work explores Cornell’s May suicide from a chronobiologic perspective. Methods: Review of Cornell’s lyrics and literature on suicide. Results: Cornell’s lyrics contain clear indicators of mixed depressive and seasonal imagery, highlighting 3 fundamental axioms of suicidology: (1) the yearly suicide rhythm peaks in May in the northern hemisphere, (2) mixed depressive states are particularly lethal, and (3) the suicide risk increases dramatically when recovering from depression and mood turns mixed. Conclusions: Cornell, in his life and music, left us with a novel and important hypothesis about the spring seasonality of suicide, namely, that the yearly suicide risk becomes maximal when winter turns to spring and there emerges a deadly mixed mood state under a May photoperiod, i.e., the suicide risk is maximal when a Black Hole Sun occurs in May. It is hoped that Cornell’s legacy and sensitive hypothesis inspire research into the etiology and treatment of the spring seasonality of suicide risk and mixed mood states. Limitations: The Cornell hypothesis was formulated based in part on several speculative inferences regarding the course of his functioning just prior to his suicide.

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A highly tunable dopaminergic oscillator generates ultradian rhythms of behavioral arousal

Cited by 145 publications

References 83 publications

Changes in Brain Monoamines Underlie Behavioural Disruptions after Zebrafish Diet Exposure to Polycyclic Aromatic Hydrocarbons Environmental Mixtures

Changes in Brain Monoamines Underlie Behavioural Disruptions after Zebrafish Diet Exposure to Polycyclic Aromatic Hydrocarbons Environmental Mixtures

The mood stabilizer valproic acid opposes the effects of dopamine on circadian rhythms

Chris Cornell, the Black Hole Sun, and the Seasonality of Suicide

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