Opposing effects of acute and chronic d-amphetamine on decision-making in rats

Wong, Scott A.; Thapa, Raj Kumar; Badenhorst, Cecilia A.; Briggs, Alicia R.; Sawada, Justan A.; Gruber, Aaron J.

doi:10.1016/j.neuroscience.2016.04.021

Cited by 17 publications

(10 citation statements)

References 69 publications

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“…Dopamine depletion in this structure drastically reduces engagement in instrumental responding (Nicola, 2010), and NACc neurons encode nearby manipulanda and presumably support approach (Morrison et al, 2015). Moreover, infusion of amphetamine into NACc increased EFS (Wong et al, 2017a), consistent with reports that this manipulation increases Pavlovian conditioned approach (Parkinson et al, 1999; du Hoffmann and Nicola, 2014). It was thus surprising that lesions of NACc in this study did not decrease EFS.…”

Section: Discussionsupporting

confidence: 89%

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Feeder Approach between Trials Is Increased by Uncertainty and Affects Subsequent Choices

Gruber

Thapa

Randolph

2017

eNeuro

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Animals quickly learn to approach sources of food. Here, we report on a form of approach in which rats made volitional orofacial contact with inactive feeders between trials of a self-paced operant task. This extraneous feeder sampling (EFS) was never reinforced and therefore imposed an opportunity and effort cost. EFS decreased during initial training but persisted thereafter. The relative rate of EFS to operant responding increased with novel changes to the operant chamber, reward devaluation by prefeeding, or lesions to the dorsolateral striatum. We speculate that this may function to increase exploration when the task is uncertain (early in learning or introduction of novel apparatus components), when the opportunity cost is low, or when the learned sensorimotor solution is compromised. Moreover, EFS strongly affected subsequent choices by triggering a lose-shift response away from the sampled feeder, even though it occurred outside of the trial context. This indicates that at least some behaviors occurring between trials impact future behaviors and should be considered in decision-making studies.

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Section: Discussionsupporting

confidence: 89%

“…EFS is modulated by drugs such as d -amphetamine (Wong et al, 2017a), but not others such as Δ-9-tetrahydrocannabinol (Wong et al, 2017b). Moreover, it appears to be sexually dimorphic in rats and may be subject to modulation by stress, inflammation, or other factors (unpublished observations).…”

Section: Discussionmentioning

confidence: 99%

Feeder Approach between Trials Is Increased by Uncertainty and Affects Subsequent Choices

Gruber

Thapa

Randolph

2017

eNeuro

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“…Sams-Dodd, 1998), an effect we observed here. Moreover, AMPH has been shown to decrease 582 feeding (Foltin, 2001;Shoblock et al, 2003;Cannon et al, 2004;Wellman et al, 2009) and 583 sensitivity to reward omission (Wong et al, 2017). Consistent with these data, we found that 584 animals spent less time at feeders, and were more likely to forgo the reward, as AMPH 585 increased.…”

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confidence: 81%

Amphetamine reduces utility encoding and stabilizes neural dynamics in rat anterior cingulate cortex

Gruber

Hashemnia

Euston

2020

Preprint

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The anterior cingulate cortex (ACC) appears to support decisions by encoding the effort-reward utility of choice options. We show here that d-amphetamine (AMPH) has dose-dependent effects on this encoding and on neural dynamics in rat ACC that are concordant with its behavioral effects. Low-dose AMPH increased task engagement and had mild effects on neural encoding, whereas high doses disrupted utility signaling and decreased task engagement. The disruption involved reduced reward signaling and compressed effort-reward encoding of utility cells, which corresponded with reduced reward consumption behaviors. Furthermore, low-dose AMPH stabilized and accelerated trajectories of neural activity in state-space, whereas high-dose AMPH destabilized trajectories. We propose that low-dose AMPH increases both excitability and stability, which preserves information and accelerates evolution of a neural ‘script’ for task execution. Excessive excitability at high doses overcomes stability enhancement to suppress weakly encoded features (e.g. reward) and cause deviation from the script, which interrupts task performance.Significance StatementAmphetamine reduced reward signaling by individual neurons in rat prefrontal cortex, but increased the stability of ensemble dynamics. These effects account for animals’ increased task engagement, despite reduced reward intake.

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“…Therefore, the disruptions in omission likely reflected a true attentional deficit. Psychostimulants, such as amphetamine ( Wong et al, 2016 ), cocaine ( Dandy and Gatch, 2009 ), and nicotine ( Kirshenbaum et al, 2011 ), had been reported to affect impulsive behavior. Acute morphine was found to cause dose-dependent increases in premature responding and decreases in perseverative responding on 5-CSRTT ( Pattij et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

The Role of Dopamine D1 and D3 Receptors in N-Methyl-D-Aspartate (NMDA)/GlycineB Site-Regulated Complex Cognitive Behaviors following Repeated Morphine Administration

Wang

Yin

Guo

et al. 2017

International Journal of Neuropsychopharmacology

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Background:Opiate addiction is associated with complex cognitive impairment, which contributes to the development of compulsive drug use and relapses. Dopamine and N-methyl-D-aspartate receptors play critical roles in opiate-induced cognitive deficits. However, the roles of D1 and D3 receptors in the N-methyl-D-aspartate/glycineB receptor-regulated cognitive behaviors induced by morphine remain unknown.Methods:The 5-choice serial reaction time task was used to investigate the cognitive profiles associated with repeated morphine administration in D1 (D1-/-)- and D3 (D3-/-)-receptor knockout mice. The expression of phosphorylated NR1, Ca2+/calmodulin-dependent protein kinase II (CaMKII), and cAMP response element-binding protein (CREB) in the brain was examined by western blotting. D1-/- and D3-/- mice were treated with the N-methyl-D-aspartate/glycineB site agonist l-aminocyclopropanecarboxylic acid and the antagonist L-701,324 to chronically disrupt N-methyl-D-aspartate receptor function and investigate their effects on morphine-induced cognitive changes.Results:Repeated morphine administration impaired attentional function and caused impulsive and compulsive behaviors. D1-/- mice exhibited hardly any premature nosepokes. D3-/- mice showed robustly increased morphine-induced impulsive behavior. The numbers of premature responses were decreased by L-701,324 administration and increased by ACPC administration; these effects were completely abolished in D1-/- mice due to their inability to perform reward-based tasks. In contrast, the inhibitory effects of L-701,324 on impulsive behavior were significantly augmented in D3-/- mice.Conclusions:N-methyl-D-aspartate/glycineB site functions may contribute to morphine-induced cognitive deficits, especially those related to impulsive behavior. D1 and D3 receptors may have contrasting effects with respect to modulating impulsive behavior. D3 receptors have inhibitory effects on impulsive behaviors, and these effects are clearly mediated by N-methyl-D-aspartate/glycineB receptor and μ-opioid receptor interactions.

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Opposing effects of acute and chronic d-amphetamine on decision-making in rats

Cited by 17 publications

References 69 publications

Feeder Approach between Trials Is Increased by Uncertainty and Affects Subsequent Choices

Feeder Approach between Trials Is Increased by Uncertainty and Affects Subsequent Choices

Amphetamine reduces utility encoding and stabilizes neural dynamics in rat anterior cingulate cortex

The Role of Dopamine D1 and D3 Receptors in N-Methyl-D-Aspartate (NMDA)/GlycineB Site-Regulated Complex Cognitive Behaviors following Repeated Morphine Administration

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