The neural basis of reversal learning: An updated perspective

Izquierdo, Alicia; Brigman, Jonathan L.; Radke, Anna K.; Rudebeck, Peter H.; Holmes, Andrew

doi:10.1016/j.neuroscience.2016.03.021

Cited by 486 publications

(489 citation statements)

References 218 publications

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“…Long-lasting sensitization in adulthood following adolescent MPH exposure found by Shanks et al (2015) may also partially explain the pattern of results we observe here. Rats may be more reward sensitive in adulthood (to natural reinforcers, such as food) following chronic developmental exposure to MPH, which may attenuate or alter learning from feedback when such learning matters most to accurate performance, in early reversal learning (Izquierdo et al 2016). …”

Section: Discussionmentioning

confidence: 99%

Sex differences, learning flexibility, and striatal dopamine D1 and D2 following adolescent drug exposure in rats

Izquierdo

Pozos

Torre

et al. 2016

Behavioural Brain Research

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Corticostriatal circuitry supports flexible reward learning and emotional behavior from the critical neurodevelopmental stage of adolescence through adulthood. It is still poorly understood how prescription drug exposure in adolescence may impact these outcomes in the long-term. We studied adolescent methylphenidate (MPH) and fluoxetine (FLX) exposure in rats and their impact on learning and emotion in adulthood. In Experiment 1, male and female rats were administered MPH, FLX, or saline (SAL), and compared with methamphetamine (mAMPH) treatment beginning in postnatal day (PND) 37. The rats were then tested on discrimination and reversal learning in adulthood. In Experiment 2, animals were administered MPH or SAL also beginning in PND 37 and later tested in adulthood for anxiety levels. In Experiment 3, we analyzed striatal dopamine D1 and D2 receptor expression in adulthood following either extensive learning (after Experiment 1) or more brief emotional measures (after Experiment 2). We found sex differences in discrimination learning and attenuated reversal learning after MPH and only sex differences in adulthood anxiety. In learners, there was enhanced striatal D1, but not D2, after either adolescent MPH or mAMPH. Lastly, also in learners, there was a sex x treatment group interaction for D2, but not D1, driven by the MPH-pretreated females, who expressed significantly higher D2 levels compared to SAL. These results show enduring effects of adolescent MPH on reversal learning in rats. Developmental psychostimulant exposure may interact with learning to enhance D1 expression in adulthood, and affect D2 expression in a sex-dependent manner.

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Section: Discussionmentioning

confidence: 99%

Sex differences, learning flexibility, and striatal dopamine D1 and D2 following adolescent drug exposure in rats

Izquierdo

Pozos

Torre

et al. 2016

Behavioural Brain Research

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“…choose based on an odor and ignore spatial location or choose based on spatial location and ignore odor) while the orbitofrontal cortex is required for reversing choices within a rule (Birrell and Brown 2000; McAlonan and Brown 2003). Neurotransmitters including dopamine, serotonin, and noradrenaline have similarly been identified to differentially contribute to behavioral flexibility in various brain regions (Kehagia et al 2010; Izquierdo et al 2016). For example, serotonergic lesions using 5,7-dihydroxytryptamine in the prefrontal cortex of monkeys impairs reversal learning but does not affect set-shifting (Clarke et al 2005).…”

Section: The Lhb Within a Broader Neural Circuitry Underlying Behamentioning

confidence: 99%

Control of behavioral flexibility by the lateral habenula

Baker

Mizumori

2017

Pharmacology Biochemistry and Behavior

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The ability to rapidly switch behaviors in dynamic environments is fundamental to survival across species. Recognizing when an ongoing behavioral strategy should be replaced by an alternative one requires the integration of a diverse number of cues both internal and external to the organism including hunger, stress, or the presence of reward predictive cues. Increasingly sophisticated behavioral paradigms coupled with state of the art electrophysiological and pharmacological approaches have delineated a brain circuit involved in behavioral flexibility. However, how diverse contextual cues are integrated to influence strategy selection on a trial by trial basis remains largely unknown. One promising candidate for integration of internal and external cues to determine whether an ongoing behavioral strategy is appropriate is the lateral habenula (LHb). The LHb receives input from many brain areas that signal both internal and external environmental contexts and in turn projects to areas involved in behavioral monitoring and plasticity. This review examines how these connections, combined with recent pharmacological and electrophysiological results reveal a critical role for the LHb in behavioral flexibility in dynamic environments. This proposed role extends the known contributions of the LHb to motivated behaviors and suggests that the fundamental role of the LHb in these behaviors goes beyond signaling rewards and punishments to dopaminergic systems.

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“…1 A and B) while they were performing a deterministic three-choice reversal learning task (22,23) (Fig. 1C).…”

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confidence: 99%

Pallidal spiking activity reflects learning dynamics and predicts performance

Schechtman

Noblejas

Mizrahi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The basal ganglia (BG) network has been divided into interacting actor and critic components, modulating the probabilities of different state-action combinations through learning. Most models of learning and decision making in the BG focus on the roles of the striatum and its dopaminergic inputs, commonly overlooking the complexities and interactions of BG downstream nuclei. In this study, we aimed to reveal the learning-related activity of the external segment of the globus pallidus (GPe), a downstream structure whose computational role has remained relatively unexplored. Recording from monkeys engaged in a deterministic three-choice reversal learning task, we found that changes in GPe discharge rates predicted subsequent behavioral shifts on a trial-by-trial basis. Furthermore, the activity following the shift encoded whether it resulted in reward or not. The frequent changes in stimulus-outcome contingencies (i.e., reversals) allowed us to examine the learning-related neural activity and show that GPe discharge rates closely matched across-trial learning dynamics. Additionally, firing rates exhibited a linear decrease in sequences of correct responses, possibly reflecting a gradual shift from goal-directed execution to automaticity. Thus, modulations in GPe spiking activity are highest for attentiondemanding aspects of behavior (i.e., switching choices) and decrease as attentional demands decline (i.e., as performance becomes automatic). These findings are contrasted with results from striatal tonically active neurons, which show none of these task-related modulations. Our results demonstrate that GPe, commonly studied in motor contexts, takes part in cognitive functions, in which movement plays a marginal role.basal ganglia | learning | attention | globus pallidus | actor-critic model T he basal ganglia have long been implicated in learning new skills and associations (1). One of the most influential models of these structures distinguishes between two domains: the main axis, whose function is to execute and choose between different actions based on their expected outcome, and the neuromodulators, which act to shape the connectivity within said axis by incorporating information regarding the results of actions on the internal and external state. These components are aptly named the actor and critic, respectively (2).The roles of the striatum, the largest structure in the main axis, and dopamine, the key neuromodulator serving as a critic in the basal ganglia framework, have been thoroughly studied. Dopamine modifies the efficacy of the corticostriatal synapses, as well as the striatal excitability directly, using signals that incorporate both expectation and external gains and losses (3-5). Decades of research have revealed the manner in which signals relaying information concerning expected and actual gains and costs are incorporated in the striatal dynamic system (6-9). However, these dopamine-and striato-centric views often fail to take into account our current understanding of the basal ganglia, which ac...

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The neural basis of reversal learning: An updated perspective

Cited by 486 publications

References 218 publications

Sex differences, learning flexibility, and striatal dopamine D1 and D2 following adolescent drug exposure in rats

Sex differences, learning flexibility, and striatal dopamine D1 and D2 following adolescent drug exposure in rats

Control of behavioral flexibility by the lateral habenula

Pallidal spiking activity reflects learning dynamics and predicts performance

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