Burst activation of dopamine neurons produces prolonged post-burst availability of actively released dopamine

Lohani, Sweyta; Martig, Adria K.; Underhill, Suzanne M.; DeFrancesco, Alicia S.; Roberts, Melanie J.; Rinaman, Linda; Amara, Susan G.; Moghaddam, Bita

doi:10.1038/s41386-018-0088-7

Cited by 39 publications

(34 citation statements)

References 86 publications

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“…The VTA receives major inhibitory GABAergic innervation from the nucleus accumbens as well as other areas in the brain ( Jhou et al., 2009a ; Jhou et al., 2009b ) that controls their patterns in firing ( Paladini and Tepper, 1999 ; Lobb et al., 2010 ) and contributes to burst activation and prolonged activity of DA neurons in the nucleus accumbens and prefrontal cortex ( Paladini et al., 2003 ; Jhou et al., 2009a ; Lobb et al., 2010 ; Morikawa and Paladini, 2011 ; Lohani et al., 2018 ). Since burst-firing can result in increased efficacy and enhanced neurotransmitter release in the presynaptic terminal ( Fisher et al., 1997 ; Floresco et al., 2003 ), GABAergic regulation of DA bursting activity is one way to modulate reward-related memories.…”

Section: Reward Memorymentioning

confidence: 99%

α1-Adrenergic Receptors in Neurotransmission, Synaptic Plasticity, and Cognition

Perez

2020

Front. Pharmacol.

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a 1-adrenergic receptors are G-Protein Coupled Receptors that are involved in neurotransmission and regulate the sympathetic nervous system through binding and activating the neurotransmitter, norepinephrine, and the neurohormone, epinephrine. There are three a 1-adrenergic receptor subtypes (a 1A , a 1B , a 1D) that are known to play various roles in neurotransmission and cognition. They are related to two other adrenergic receptor families that also bind norepinephrine and epinephrine, the band a 2-, each with three subtypes (b 1 , b 2 , b 3 , a 2A , a 2B , a 2C). Previous studies assessing the roles of a 1-adrenergic receptors in neurotransmission and cognition have been inconsistent. This was due to the use of poorly-selective ligands and many of these studies were published before the characterization of the cloned receptor subtypes and the subsequent development of animal models. With the availability of more-selective ligands and the development of animal models, a clearer picture of their role in cognition and neurotransmission can be assessed. In this review, we highlight the significant role that the a 1-adrenergic receptor plays in regulating synaptic efficacy, both short and long-term synaptic plasticity, and its regulation of different types of memory. We will also present evidence that the a 1-adrenergic receptors, and particularly the a 1A-adrenergic receptor subtype, are a potentially good target to treat a wide variety of neurological conditions with diminished cognition.

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Section: Reward Memorymentioning

confidence: 99%

α1-Adrenergic Receptors in Neurotransmission, Synaptic Plasticity, and Cognition

Perez

2020

Front. Pharmacol.

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“…Tonic dopamine has been suggested to reflect an average reward signal computed by slow averaging phasic prediction error signals (Niv et al, 2007): cues that have been associated with higher reward expectancies induce larger phasic positive prediction errors resulting in transient increases in tonic dopamine (Phillips and Wightman, 2004; Tobler et al, 2005). Although it has often been suggested that tonic and phasic dopamine are mediated by distinct mechanisms (Floresco et al, 2003; Bromberg-Martin et al, 2010), recent data demonstrated that phasic dopamine could trigger secondary events that increase tonic activation of dopamine levels (Lohani et al, 2018). It is therefore tempting to think that phasic dopamine signaling associated with higher reward expectancies or action values in context-specific perceived control, could influence general perceived control reflected by changes in tonic dopamine levels.…”

Section: Reward Rate Tonic Dopamine and (General) Perceived Controlmentioning

confidence: 99%

A Reward-Based Framework of Perceived Control

Wang

Bhanji

et al. 2019

Front. Neurosci.

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Perceived control can be broadly defined as the belief in one’s ability to exert control over situations or events. It has long been known that perceived control is a major contributor toward mental and physical health as well as a strong predictor of achievements in life. However, one issue that limits a mechanistic understanding of perceived control is the heterogeneity of how the term is defined in models in psychology and neuroscience, and used in experimental settings across a wide spectrum of studies. Here, we propose a framework for studying perceived control by integrating the ideas from traditionally separate work on perceived control. Specifically, we discuss key properties of perceived control from a reward-based framework, including choice opportunity, instrumental contingency, and success/reward rate. We argue that these separate reward-related processes are integral to fostering an enhanced perception of control and influencing an individual’s behavior and well-being. We draw on select studies to elucidate how these reward-related elements are implicated separately and collectively in the investigation of perceived control. We highlight the role of dopamine within corticostriatal pathways shared by reward-related processes and perceived control. Finally, through the lens of this reward-based framework of perceived control, we consider the implications of perceived control in clinical deficits and how these insights could help us better understand psychopathology and treatment options.

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“…Prior work has suggested that cortical inputs in response to task-related cues (i.e., phasiclike responses) regulates VTA engagement . Furthermore, recent rodent research shows that phasic increases in dopamine signaling can increase statedependent engagement of the mesolimbic system for prolonged periods of time (Lohani et al, 2018). These findings suggest that age-related differences in the cortical detection of task-relevant cues may be associated with downstream engagement of statedependent functional coupling.…”

Section: Significance Statementmentioning

confidence: 91%

“…Previous research has demonstrated that the detection of behavioral cues by cortex regulate the functional engagement of the VTA (Murty et al, 2017) and VTA-NAcc coupling (Ballard et al, 2011) and that phasic engagement of the VTA can lead to prolonged activation of mesolimbic systems (Lohani et al, 2018). Given that adolescence may be associated with enhanced sensitivity to goal-relevant information in the environment, we characterized relationships between cue-related activation and our state-dependent increases in VTA-NAcc coupling.…”

Section: Moderators Of State-dependent Neurodevelopmentmentioning

confidence: 99%

Age-Related Trajectories of Functional Coupling between the VTA and Nucleus Accumbens Depend on Motivational State

Murty

Shah

Montez³

et al. 2018

J. Neurosci.

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Over-engagement of the mesolimbic dopamine system is thought to enhance motivation in adolescents. Whereas human neuroimaging has characterized event-evoked responses of the mesolimbic system in adolescents, research has yet to characterize state-dependent engagement (i.e., seconds to minutes) of this system in goal-relevant contexts. In the current longitudinal study, we characterized age-related changes in state-dependent coupling in male and female human participants ranging in age from adolescence to adulthood. Analyses focused on two key regions of the mesolimbic dopamine system, the ventral tegmental area (VTA) and nucleus accumbens (NAcc). Although there were no differences in VTA-NAcc functional coupling in a resting-state context, VTA-NAcc functional coupling was enhanced in preadolescence/early adolescence and decreased into adulthood in a motivational context, in which individuals had to translate goal-relevant cues into instrumental actions. Furthermore, we found that task-related activation in orbitofrontal cortex, middle temporal gyrus, and visual association cortex partially mediated age-related changes in state-dependent VTA-NAcc functional coupling. These results extend prior models of neurodevelopment by showing a relationship between cortical event-evoked activation and state-dependent increases in subcortical engagement of mesolimbic systems. Adolescence is characterized by increased motivated behavior, which is thought to result from an over-engagement of mesolimbic dopamine systems. Rodent models show increases in state-dependent engagement of mesolimbic systems in adolescence. However, human neuroimaging research has mainly focused on event-evoked responses (i.e., reward cues). We show that in motivational contexts, there is increased state-dependent coupling across mesolimbic systems in preadolescence/early adolescence that decreases into adulthood and is further predicted by event-evoked cortical responses. Critically, these developmental trajectories were specific to motivationally relevant contexts and were not apparent during resting state. These findings extend emerging models of human development and suggest that state-dependent increases in dopamine signaling may underlie heightened motivation.

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Burst activation of dopamine neurons produces prolonged post-burst availability of actively released dopamine

Cited by 39 publications

References 86 publications

α1-Adrenergic Receptors in Neurotransmission, Synaptic Plasticity, and Cognition

α1-Adrenergic Receptors in Neurotransmission, Synaptic Plasticity, and Cognition

A Reward-Based Framework of Perceived Control

Age-Related Trajectories of Functional Coupling between the VTA and Nucleus Accumbens Depend on Motivational State

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