Neural Mechanisms of Circadian Regulation of Natural and Drug Reward

DePoy, Lauren M.; McClung, Colleen A.; Logan, Ryan W.

doi:10.1155/2017/5720842

Cited by 42 publications

(39 citation statements)

References 118 publications

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“…Drugs of abuse may also entrain cellular and molecular rhythms, leading to the anticipation of subsequent drug administration or drug paired-cue presentations involved in craving and relapse [147,148]. This opens the door to future work exploring whether DA/glutamate co-transmission may be a key process required for the energetic demands of drug-fueled changes in circadian rhythms and neuronal activity associated with reward and addictive behaviors.…”

Section: Discussionmentioning

confidence: 99%

The intertwined roles of circadian rhythmsand neuronal metabolism fueling drug reward and addiction

Freyberg

Logan

2018

Current Opinion in Physiology

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Drug addiction is a highly prevalent and devastating disorder with few effective treatments, resulting in enormous burdens on family and society. The cellular and behavioral effects of drugs of abuse are related to their abilities to elevate synaptic dopamine levels. Midbrain dopaminergic neurons projecting from the ventral tegmental area to the nucleus accumbens play crucial roles in substance-induced neural and behavioral plasticity. Significantly, increasing work suggests that interplay between the brain circadian system and the cellular bioenergetic machinery in these dopamine neurons plays a critical role in mediating the actions of drugs of abuse. Here, we describe recent progress in elucidating the interconnections between circadian and metabolic systems at the molecular and cellular levels and their relationships to modulation of drug reward and addiction.

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Section: Discussionmentioning

confidence: 99%

The intertwined roles of circadian rhythmsand neuronal metabolism fueling drug reward and addiction

Freyberg

Logan

2018

Current Opinion in Physiology

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“…The utility of a circadian system for adjusting rest-activity cycles to times of day most favorable for resource acquisition is self-evident, but it is not unreasonable to speculate that clock entrainment could support addictive behaviors. If episodes of drug, alcohol or junk food consumption are concentrated at a particular time of day (for example, evenings), circadian entrainment processes that serve to reinforce successful daily patterns of reward acquisition could contribute to the emergence, maintenance and relapse of compulsive eating, drinking or drug taking [111][112][113] . Another line of work suggests that ultradian oscillators can induce behavioral rhythms at circadian or longer intervals, depending on DA tone (manipulated, for example, by chronic methamphetamine consumption) and striatal DA levels 114 .…”

Section: Concluding Thoughtsmentioning

confidence: 99%

Food as circadian time cue for appetitive behavior

Mistlberger

2020

F1000Res

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Feeding schedules entrain circadian clocks in multiple brain regions and most peripheral organs and tissues, thereby synchronizing daily rhythms of foraging behavior and physiology with times of day when food is most likely to be found. Entrainment of peripheral clocks to mealtime is accomplished by multiple feeding-related signals, including absorbed nutrients and metabolic hormones, acting in parallel or in series in a tissue-specific fashion. Less is known about the signals that synchronize circadian clocks in the brain with feeding time, some of which are presumed to generate the circadian rhythms of food-anticipatory activity that emerge when food is restricted to a fixed daily mealtime. In this commentary, I consider the possibility that food-anticipatory activity rhythms are driven or entrained by circulating ghrelin, ketone bodies or insulin. While evidence supports the potential of these signals to participate in the induction or amount of food-anticipatory behavior, it falls short of establishing either a necessary or sufficient role or accounting for circadian properties of anticipatory rhythms. The availability of multiple, circulating signals by which circadian oscillators in many brain regions might entrain to mealtime has supported a view that food-anticipatory rhythms of behavior are mediated by a broadly distributed system of clocks. The evidence, however, does not rule out the possibility that multiple peripheral and central food-entrained oscillators and feeding-related signals converge on circadian oscillators in a defined location which ultimately set the phase and gate the expression of anticipatory activity rhythms. A candidate location is the dorsal striatum, a core component of the neural system which mediates reward, motivation and action and which contains circadian oscillators entrainable by food and dopaminergic drugs. Systemic metabolic signals, such as ghrelin, ketones and insulin, may participate in circadian food anticipation to the extent that they modulate dopamine afferents to circadian clocks in this area.

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“…Circadian rhythm disturbances are linked to the development and progression of neuropsychiatric illnesses, including sub-stance use disorders (Logan et al, 2014). Perturbations of the circadian system may contribute to the vulnerability for substance use (DePoy et al, 2017;Logan et al, 2018). Moreover, human genetic studies associate circadian gene variants and polymorphisms with mood and addiction disorders (McCarthy and Welsh, 2012;Shumay et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Cell-Type-Specific Regulation of Nucleus Accumbens Synaptic Plasticity and Cocaine Reward Sensitivity by the Circadian Protein, NPAS2

et al. 2019

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The circadian transcription factor neuronal PAS domain 2 (NPAS2) is linked to psychiatric disorders associated with altered reward sensitivity. The expression of Npas2 is preferentially enriched in the mammalian forebrain, including the nucleus accumbens (NAc), a major neural substrate of motivated and reward behavior. Previously, we demonstrated that downregulation of NPAS2 in the NAc reduces the conditioned behavioral response to cocaine in mice. We also showed that Npas2 is preferentially enriched in dopamine receptor 1 containing medium spiny neurons (D1R-MSNs) of the striatum. To extend these studies, we investigated the impact of NPAS2 disruption on accumbal excitatory synaptic transmission and strength, along with the behavioral sensitivity to cocaine reward in a cell-type-specific manner. Viral-mediated knockdown of Npas2 in the NAc of male and female C57BL/6J mice increased the excitatory drive onto MSNs. Using Drd1a-tdTomato mice in combination with viral knockdown, we determined these synaptic adaptations were specific to D1R-MSNs relative to non-D1R-MSNs. Interestingly, NAc-specific knockdown of Npas2 blocked cocaine-induced enhancement of synaptic strength and glutamatergic transmission specifically onto D1R-MSNs. Last, we designed, validated, and used a novel Cre-inducible short-hairpin RNA virus for MSN-subtype-specific knockdown of Npas2. Cell-type-specific Npas2 knockdown in D1R-MSNs, but not D2R-MSNs, in the NAc reduced cocaine conditioned place preference. Together, our results demonstrate that NPAS2 regulates excitatory synapses of D1R-MSNs in the NAc and cocaine reward-related behavior.

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Neural Mechanisms of Circadian Regulation of Natural and Drug Reward

Cited by 42 publications

References 118 publications

The intertwined roles of circadian rhythmsand neuronal metabolism fueling drug reward and addiction

The intertwined roles of circadian rhythmsand neuronal metabolism fueling drug reward and addiction

Food as circadian time cue for appetitive behavior

Cell-Type-Specific Regulation of Nucleus Accumbens Synaptic Plasticity and Cocaine Reward Sensitivity by the Circadian Protein, NPAS2

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