Altered Risk-Based Decision Making following Adolescent Alcohol Use Results from an Imbalance in Reinforcement Learning in Rats

Clark, Jeremy J.; Nasrallah, Nicholas A.; Hart, Andrew S.; Collins, Anne L.; Bernstein, Ilene L.; Phillips, Paul E. M.

doi:10.1371/journal.pone.0037357

Cited by 29 publications

(56 citation statements)

References 34 publications

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“…We have further demonstrated that increased risk preference may result from a selective defect in reinforcement learning (Clark et al, 2012) and that this is a specific consequence of alcohol exposure during adolescence, as identical exposure in adults does not produce this effect (Schindler et al, 2014). The mesolimbic dopamine system is implicated in reinforcement learning, goal-directed behavior, and motivational processes, including those for abused substances (Everitt and Robbins, 2005;Kelley, 2004;Robinson and Berridge, 1993;Salmone and Correa, 2012;Schultz, 2007).…”

Section: Introductionmentioning

confidence: 79%

“…The gelatin was made available 24 h/day in addition to ad libitum water and chow, and the jars were replaced with fresh gelatin every day. Alcohol and control gelatin was prepared as previously described (Clark et al, 2012;Nasrallah et al, 2009). Upon completion of the 20-day alcohol and control exposure, jars were removed and the rats were monitored daily for withdrawal symptoms.…”

Section: Alcohol Administrationmentioning

confidence: 99%

“…Pavlovian conditioning in a wide variety of species has been shown to elicit alternative conditioned responses where some individuals engage with the stimulus itself during cue presentation (sign trackers) and other individuals engage the site of reward delivery during cue presentation (goal trackers) (Boakes, 1977;Robinson and Flagel, 2009). The sign-tracking response is accompanied by a dynamic pattern of dopamine release in the ventral striatum, is dopamine dependent, and has been interpreted as being indicative of a learning strategy where incentive value is assigned to reward-predictive cues (Clark et al, 2012;Flagel et al, 2011). Importantly, individuals who attribute greater incentive value to reward-predictive cues during Pavlovian conditioning with natural rewards go on to exhibit greater cue-evoked motivational responses to drug-associated cues during cocaine self-administration .…”

Section: Introductionmentioning

confidence: 99%

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Adolescent Alcohol Exposure Amplifies the Incentive Value of Reward-Predictive Cues Through Potentiation of Phasic Dopamine Signaling

Spoelder

Tsutsui

Lesscher

et al. 2015

Neuropsychopharmacol

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Adolescent alcohol use remains a major public health concern due in part to well-established findings implicating the age of onset in alcohol use in the development of alcohol use disorders and persistent decision-making deficits in adults. We have previously demonstrated that moderate adolescent alcohol consumption in rats promotes suboptimal decision making and an associated perturbation in mesolimbic dopamine transmission in adulthood. Dopamine-dependent incentive learning processes are an integral component of value-based decision making and a fundamental element to many theoretical accounts of addiction. Thus we tested the hypothesis that adolescent alcohol use selectively alters incentive learning processes through perturbation of mesolimbic dopamine systems. To assess incentive learning, behavioral and neurochemical measurements were made during the acquisition, maintenance, extinction, and reacquisition of a Pavlovian conditioned approach procedure in adult rats with a history of adolescent alcohol consumption. We show that moderate adolescent alcohol consumption potentiates stimulus-evoked phasic dopamine transmission, measured in vivo by fast-scan cyclic voltammetry, in adulthood and biases individuals toward a dopamine-dependent incentive learning strategy. Moreover, we demonstrate that animals exposed to alcohol in adolescence are more sensitive to an unexpected variation in reward outcomes. This pattern of phasic dopamine signaling and the associated bias in learning may provide a mechanism for the well-documented vulnerability of individuals with early-life alcohol use for alcohol use disorders in adulthood.

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Section: Introductionmentioning

confidence: 79%

Section: Alcohol Administrationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Adolescent Alcohol Exposure Amplifies the Incentive Value of Reward-Predictive Cues Through Potentiation of Phasic Dopamine Signaling

Spoelder

Tsutsui

Lesscher

et al. 2015

Neuropsychopharmacol

View full text Add to dashboard Cite

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“…Still, it is alarming that even moderate levels of intake, when consumed chronically during adolescence, exerted significant effects on both behavior and neurophysiology. While the gelatin vehicle used here is becoming increasingly common (Clark et al, 2012;Nasrallah et al, 2009Nasrallah et al, , 2011Peris et al, 2006), it is still a relatively new consumption model. In our hands, animals consuming control gelatin ate considerably more gelatin than both the alcohol groups.…”

Section: Discussionmentioning

confidence: 99%

“…Here, following the adolescent period, alcohol was no longer given to rats, and we examined preferences for risky payoffs across a range of probabilities, while simultaneously recording OFC activity using in vivo electrophysiology. Previous studies have shown enhanced risk-preference associated with altered neural signaling following similar adolescent alcohol consumption (Clark et al, 2012;Nasrallah et al, 2009Nasrallah et al, , 2011. We therefore hypothesized that greater modulation of OFC activity in response to rewards under conditions of risk would be associated with enhanced preference for the risky choice option across levels of risk.…”

Section: Introductionmentioning

confidence: 98%

Consequences of Adolescent Ethanol Consumption on Risk Preference and Orbitofrontal Cortex Encoding of Reward

McMurray

Amodeo

Roitman

2015

Neuropsychopharmacol

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Critical development of the prefrontal cortex occurs during adolescence, a period of increased independence marked by decision making that often includes engagement in risky behaviors, such as substance use. Consumption of alcohol during adolescence has been associated with increased impulsivity that persists across the lifespan, an effect which may be caused by long-term disruptions in cortical processing of rewards. To determine if alcohol consumption alters cortical encoding of rewards of different sizes and probabilities, we gave rats limited access to alcohol in gelatin during adolescence only. In adulthood, we recorded the electrophysiological activity of individual neurons of the orbitofrontal cortex while rats performed a risk task that varied the level of risk from day-to-day. Rats that had consumed higher levels of alcohol showed increased risk preference in the task compared with control and low alcohol-consuming rats. Patterns of neuronal responses were identified using principal component analysis. Of the multiple patterns observed, only one was modulated by adolescent alcohol consumption and showed strongest modulation after reward receipt. This subpopulation of neurons showed blunted firing rates following rewards in alcohol-consuming rats, suggesting a mechanism through which adolescent alcohol exposure may have lasting effects on reward processing in the context of decision making. The differences in OFC responses between high alcohol consumers and control animals not given access to alcohol support the idea that, regardless of potential variability in innate alcohol preferences, voluntary consumption of alcohol during adolescence biases choice patterns longitudinally through alterations in cortical function.

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Adolescent Drinking and Motivated Decision-Making: A Cotwin-Control Investigation with Monozygotic Twins

et al. 2014

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The present study used a monozygotic (MZ) cotwin-control (CTC) design to investigate associations between alcohol use and performance on the Iowa Gambling Task (IGT) in a sample of 96 adolescents (half female). The MZ CTC design is well suited to shed light on whether poor decision-making, as reflected on IGT performance, predisposes individuals to abuse substances or is a consequence of use. Participants completed structural MRI scans as well, from which we derived gray matter volumes for cortical and subcortical regions involved in IGT performance and reduced in adolescents with problematic alcohol use. Drinking was associated with poorer task performance and with reduced volume of the left lateral orbital-frontal cortex. CTC analyses indicated that the former was due to differences between members of twin pairs in alcohol use (suggesting a causal effect of alcohol), whereas the latter was due to factors shared by twins (consistent with a pre-existing vulnerability for use). Although these preliminary findings warrant replication, they suggest that normative levels of alcohol use may diminish the quality of adolescent decision-making and thus have potentially important public health implications.

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Altered Risk-Based Decision Making following Adolescent Alcohol Use Results from an Imbalance in Reinforcement Learning in Rats

Cited by 29 publications

References 34 publications

Adolescent Alcohol Exposure Amplifies the Incentive Value of Reward-Predictive Cues Through Potentiation of Phasic Dopamine Signaling

Adolescent Alcohol Exposure Amplifies the Incentive Value of Reward-Predictive Cues Through Potentiation of Phasic Dopamine Signaling

Consequences of Adolescent Ethanol Consumption on Risk Preference and Orbitofrontal Cortex Encoding of Reward

Adolescent Drinking and Motivated Decision-Making: A Cotwin-Control Investigation with Monozygotic Twins

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