Diurnal rhythms in cholinergic modulation of rapid dopamine signals and associative learning in the striatum

Stowe, Taylor A.; Pitts, Elizabeth G.; Leach, Amy C.; Iacino, Melody; Niere, Farr; Graul, Benjamin; Raab‐Graham, Kimberly F.; Yorgason, Jordan T.; Ferris, Mark J.

doi:10.1016/j.celrep.2022.110633

Cited by 13 publications

(7 citation statements)

References 53 publications

(75 reference statements)

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“…Several studies have shown that nearly all aspects of dopamine transmission, including synaptic dopamine release, DAT activity, expression of dopamine receptors, dopamine synthesis and dopamine-dependent behaviors show diurnal rhythms (Naber et al, 1980;Schade et al, 1995;Akhisaroglu et al, 2005;Sleipness et al, 2007;Ferris et al, 2014;Stowe et al, 2022). Experiments in the present study were conducted during the mid-light phase of each photoperiod where synaptic dopamine release and DAT function are predicted to be at their peak (Ferris et al, 2014).…”

Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 95%

“…NAc core dopamine is highly involved in reinforcement learning (Tsai et al, 2009;Floresco et al, 2015;Kutlu et al, 2021), and our data predicts that photoperiod could drive differences in female reinforcement behaviors such as reward responding, acquisition, and motivation through modulation of NAc core dopamine. Stowe et al 2022 demonstrated that the diurnal rhythm of sign-tracking behavior is synchronous with diurnal rhythms of phasic/tonic ratio of electrically evoked NAc core dopamine. Sign-tracking is an associative learning behavior dependent on NAc dopamine that is linked to addiction-related behaviors (Robinson et al, 2014).…”

Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 95%

“…Cholinergic interneurons (CINs) in the NAc can enhance and even directly elicit dopamine release from terminals in the NAc through presynaptic nicotinic acetylcholine receptors (Yorgason et al, 2017). There is evidence that NAc CIN activity is diurnal and drives diurnal rhythms of NAc dopamine release (Stowe et al, 2022), so it is possible that CIN firing rate may be responsive to photoperiod. Another possible mechanism through which photoperiod could affect dopamine release is through regulation of D2 dopamine autoreceptors.…”

Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 99%

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Photoperiod Impacts Nucleus Accumbens Dopamine Dynamics

Jameson

Siemann

Melchior

et al. 2023

eNeuro

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Circadian photoperiod, or day length, changes with the seasons and influences behavior to allow animals to adapt to their environment. Photoperiod is also associated with seasonal rhythms of affective state, as evidenced by seasonality of several neuropsychiatric disorders. Interestingly, seasonality tends to be more prevalent in women for affective disorders such as Major Depressive Disorder and Bipolar Disorder. However, the underlying neurobiological processes contributing to sex-linked seasonality of affective behaviors are largely unknown. Mesolimbic dopamine input to the nucleus accumbens (NAc) contributes to the regulation of affective state and behaviors. Additionally, sex differences in the mesolimbic dopamine pathway are well-established. Therefore, we hypothesize that photoperiod may drive differential modulation of NAc dopamine in males and females. Here, we used fast-scan cyclic-voltammetry (FSCV) to explore whether photoperiod can modulate sub-second dopamine signaling dynamics in the NAc core of male and female mice raised in seasonally relevant photoperiods. We found that photoperiod modulates dopamine signaling in the NAc core, and that this effect is sex-specific to females. Both release and uptake of dopamine were enhanced in the NAc core of female mice raised in long, summer-like photoperiods, whereas we did not find photoperiodic effects on NAc core dopamine in males. These findings uncover a potential neural circuit basis for sex-linked seasonality in affective behaviors.Significance StatementDay length, or photoperiod, is a reliable indicator of the changing seasons, and is a powerful environmental cue influencing affective state and behavior. While studies have shown that photoperiod can modulate neurotransmitter systems involved in affective behavior, like the dopamine system, there are few studies examining effects of photoperiod on the synaptic level. Here we assess mesolimbic dopamine dynamics in mice maintained in seasonal photoperiods. We found a sex-specific effect wherein photoperiod modulates dopamine release from and uptake in dopaminergic terminals in the nucleus accumbens core of female mice with long summer-like photoperiods increasing dopamine release, thus uncovering a potential synaptic basis for sex-linked seasonality in affective behaviors.

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Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 95%

Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 95%

Section: Long Photoperiod Enhances Dat Inhibition In Femalesmentioning

confidence: 99%

See 1 more Smart Citation

Photoperiod Impacts Nucleus Accumbens Dopamine Dynamics

Jameson

Siemann

Melchior

et al. 2023

eNeuro

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“…We treated lights off as zeitgeber time (ZT) 12 as our animal model is nocturnal, in which lights off is the relevant circadian cue. Work by Stowe et al (2022) ; Ferris et al (2014) found that diurnal rhythms of DA release peak at midday. Based on this work, and our own previous methods, we conducted all experiments at the midday time point.…”

Section: Methodsmentioning

confidence: 99%

Effects of age and sex on photoperiod modulation of nucleus accumbens monoamine content and release in adolescence and adulthood

Jameson,

Siemann,

Grueter

et al. 2024

Neurobiology of Sleep and Circadian Rhythms

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“…Recently, Stowe and colleagues showed diurnal rhythms in rapid dopamine signaling in the striatum which are mediated by time-of-day shifts in cholinergic interneuron control of dopamine. These systems work together to mediate time-of-day changes in conditioned responses to reward-associated cues ( Stowe et al, 2022 ). The major NAc projection neurons that regulate these behaviors are GABA and peptide expressing neurons, also called medium spiny neurons (MSNs).…”

Section: Ventral Tegmental Area and Nucleus Accumbensmentioning

confidence: 99%

Emotionally clocked out: cell-type specific regulation of mood and anxiety by the circadian clock system in the brain

Francis

Porcu

2023

Front. Mol. Neurosci.

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Circadian rhythms are self-sustained oscillations of biological systems that allow an organism to anticipate periodic changes in the environment and optimally align feeding, sleep, wakefulness, and the physiological and biochemical processes that support them within the 24 h cycle. These rhythms are generated at a cellular level by a set of genes, known as clock genes, which code for proteins that inhibit their own transcription in a negative feedback loop and can be perturbed by stress, a risk factor for the development of mood and anxiety disorders. A role for circadian clocks in mood and anxiety has been suggested for decades on the basis of clinical observations, and the dysregulation of circadian rhythms is a prominent clinical feature of stress-related disorders. Despite our understanding of central clock structure and function, the effect of circadian dysregulation in different neuronal subtypes in the suprachiasmatic nucleus (SCN), the master pacemaker region, as well as other brain systems regulating mood, including mesolimbic and limbic circuits, is just beginning to be elucidated. In the brain, circadian clocks regulate neuronal physiological functions, including neuronal activity, synaptic plasticity, protein expression, and neurotransmitter release which in turn affect mood-related behaviors via cell-type specific mechanisms. Both animal and human studies have revealed an association between circadian misalignment and mood disorders and suggest that internal temporal desynchrony might be part of the etiology of psychiatric disorders. To date, little work has been conducted associating mood-related phenotypes to cell-specific effects of the circadian clock disruptions. In this review, we discuss existing literature on how clock-driven changes in specific neuronal cell types might disrupt phase relationships among cellular communication, leading to neuronal circuit dysfunction and changes in mood-related behavior. In addition, we examine cell-type specific circuitry underlying mood dysfunction and discuss how this circuitry could affect circadian clock. We provide a focus for future research in this area and a perspective on chronotherapies for mood and anxiety disorders.

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Diurnal rhythms in cholinergic modulation of rapid dopamine signals and associative learning in the striatum

Cited by 13 publications

References 53 publications

Photoperiod Impacts Nucleus Accumbens Dopamine Dynamics

Photoperiod Impacts Nucleus Accumbens Dopamine Dynamics

Effects of age and sex on photoperiod modulation of nucleus accumbens monoamine content and release in adolescence and adulthood

Emotionally clocked out: cell-type specific regulation of mood and anxiety by the circadian clock system in the brain

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