Fronto-striatal gray matter contributions to discrimination learning in Parkinson's disease

O’Callaghan, Claire; Moustafa, Ahmed A.; Wit, Sanne de; Shine, James M.; Robbins, Trevor W.; Lewis, Simon J.G.; Hornberger, Michael

doi:10.3389/fncom.2013.00180

Cited by 14 publications

(16 citation statements)

References 74 publications

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“…These extends prior findings by the same authors on the effects of PD on category learning (Filoteo et al, 2007). Using imaging and computational modeling, O'Callaghan et al (2013) studied learning impairment in PD patients, showing evidence for a role for the ventromedial prefrontal cortex and inferior frontal gyrus in these processes; this extends prior findings of the role of the basal ganglia in learning processes (Bodi et al, 2009;Keri et al, 2010).…”

Section: Human Studiessupporting

confidence: 74%

Basal ganglia: physiological, behavioral, and computational studies

2015

Frontiers Research Topics

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Keywords: basal ganglia, dopamine, Parkinson's disease (PD), computational modeling, animal studies, human imaging studies, deep brain stimulationThe basal ganglia has received much attention over the last two decades, as it has been implicated in many neurological and psychiatric disorders, including Parkinson's disease (PD), Attention Deficit Hyperactivity Disorder (ADHD), Tourette's syndrome, and dystonia. Most of current basal ganglia research-in both animals and humans-attempts to understand the neural and biochemical substrates of basic motor and learning processes, and how these are affected in human patients as well as animal models of brain disorders, particularly PD.The current volume contains research articles and reviews describing basic, pre-clinical and clinical neuroscience research of the basal ganglia written by researchers of the basal ganglia and attendees of the 11th Triennial Meeting of the International Basal Ganglia Society (IBAGS) that was held on March 3-7th, 2013 at the Princess Hotel, Eilat, Israel. Specifically, articles in this volume include research reports on the biochemistry, computational theory, anatomy, and physiology of single neurons and functional circuitry of the basal ganglia networks.Below, we provide a summary of articles published in the volume. We divided the articles into 4 sections: animal studies, human studies, computational modeling, and reviews. ANIMAL STUDIESUsing physiological recordings, Adler et al. (2013) studied the relationship of both medium spiny cells and interneurons of the striatum while monkeys were performing a Pavlovian conditioning task, showing that both classes of neurons play a key role in conditioning. Along these lines, Yael et al. (2013) studied the effects of D2 antagonists (haloperidol) on striatal activity, finding evidence that it alters firing patterns of medium spiny cells and interneurons. Interestingly, Bronfeld et al. (2013) found that microinjection of the GABA A antagonist bicuculline in the dorsal striatum leads to Tourette's tics in rats, potentially highlighting a role of interneurons in such motor symptoms. However, future studies should explain the exact function of interneurons in the generation of tics. In another study, Plata et al. (2013) found that the administration of nicotine activates inhibitory interneurons in the striatum, which can treat motor symptoms of PD (as similar to dopaminergic medications). The implications of these findings remain to be shown in clinical studies. Using whole-cell patch-clamp recordings, Arias-Garcia et al. (2013) found, for the first time, that Ca 2+ -activated K + channels explain the different durations between corticostriatal responses in the basal ganglia direct and indirect pathways. Future research should explain the relationship between these findings and motor symptoms in PD.While the above studies focus on the striatum, other studies in the volume address the function of other downstream basal ganglia structures. For example, Lavian et al. (2013) studied the effects of high and...

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Section: Human Studiessupporting

confidence: 74%

Basal ganglia: physiological, behavioral, and computational studies

2015

Frontiers Research Topics

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“…Moreover, we did not quantify DA system or structural changes in frontostriatal brain areas, which have also been associated with reductions in stimulus–action–outcome learning in PD (O’Callaghan et al, 2013). These factors will be important issues to control and study in future investigations.…”

Section: Discussionmentioning

confidence: 99%

Dopamine Selectively Modulates the Outcome of Learning Unnatural Action–Valence Associations

Wouwe

Claassen

Kanoff

et al. 2017

Journal of Cognitive Neuroscience

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Learning the contingencies between stimulus, action, and outcomes is disrupted in disorders associated with altered dopamine (DA) function in the BG, such as Parkinson disease (PD). Although the role of DA in learning to act has been extensively investigated in PD, the role of DA in “learning to withhold” (or inhibit) action to influence outcomes is not as well understood. The current study investigated the role of DA in learning to act or to withhold action to receive rewarding, or avoid punishing outcomes, in patients with PD tested “off” and “on” dopaminergic medication (n = 19) versus healthy controls (n = 30). Participants performed a reward-based learning task that orthogonalized action and outcome valence (action–reward, inaction–reward, action–punishment, inaction–punishment). We tested whether DA would bias learning toward action, toward reward, or to particular action–outcome interactions. All participants demonstrated inherent learning biases preferring action with reward and inaction to avoid punishment, and this was unaffected by medication. Instead, DA produced a complex modulation of learning less natural action–outcome associations. “Off” DA medication, patients demonstrated impairments in learning to withhold action to gain reward, suggesting a difficulty to overcome a bias toward associating inaction with punishment avoidance. On DA medication, these patterns changed, and patients showed a reduced ability to learn to act to avoid punishment, indicating a bias toward action and reward. The current findings suggest that DA in PD has a complex influence on the formation of action–outcome associations, particularly those involving less natural linkages between action and outcome valence.

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“…Crucially, a devaluation sensitivity index (DSI) is calculated based on the difference in responding between these two trial types, providing a single parameter that represents the relative involvement of the habit vs. goal-directed system in action control. This task has been used extensively to study goal-directed and habitual action control in healthy participants (de Wit et al, 2009, 2012b) following dopamine (de Wit et al, 2012a) and serotonin level reductions (Worbe et al, 2015) and in patient samples, including obsessive-compulsive disorder (Gillan et al, 2011), alcohol dependence (Sjoerds et al, 2013), Gille de La Tourette syndrome (Delorme et al, 2016), Parkinson’s Disease (de Wit et al, 2011; O’Callaghan et al, 2013) and autism spectrum disorders (Geurts and de Wit, 2014). It remains unclear, however, how devaluation sensitivity, as assessed with this task, relates to other paradigms assessing goal-directed and habitual control, such as the model-based (MB) and model-free (MF) reinforcement learning (RL) algorithms used during sequential decision making.…”

Section: Introductionmentioning

confidence: 99%

Slips of Action and Sequential Decisions: A Cross-Validation Study of Tasks Assessing Habitual and Goal-Directed Action Control

Sjoerds

Dietrich

Deserno

et al. 2016

Front. Behav. Neurosci.

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Instrumental learning and decision-making rely on two parallel systems: a goal-directed and a habitual system. In the past decade, several paradigms have been developed to study these systems in animals and humans by means of e.g., overtraining, devaluation procedures and sequential decision-making. These different paradigms are thought to measure the same constructs, but cross-validation has rarely been investigated. In this study we compared two widely used paradigms that assess aspects of goal-directed and habitual behavior. We correlated parameters from a two-step sequential decision-making task that assesses model-based (MB) and model-free (MF) learning with a slips-of-action paradigm that assesses the ability to suppress cue-triggered, learnt responses when the outcome has been devalued and is therefore no longer desirable. MB control during the two-step task showed a very moderately positive correlation with goal-directed devaluation sensitivity, whereas MF control did not show any associations. Interestingly, parameter estimates of MB and goal-directed behavior in the two tasks were positively correlated with higher-order cognitive measures (e.g., visual short-term memory). These cognitive measures seemed to (at least partly) mediate the association between MB control during sequential decision-making and goal-directed behavior after instructed devaluation. This study provides moderate support for a common framework to describe the propensity towards goal-directed behavior as measured with two frequently used tasks. However, we have to caution that the amount of shared variance between the goal-directed and MB system in both tasks was rather low, suggesting that each task does also pick up distinct aspects of goal-directed behavior. Further investigation of the commonalities and differences between the MF and habit systems as measured with these, and other, tasks is needed. Also, a follow-up cross-validation on the neural systems driving these constructs across different paradigms would promote the definition and operationalization of measures of instrumental learning and decision-making in humans.

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Fronto-striatal gray matter contributions to discrimination learning in Parkinson's disease

Cited by 14 publications

References 74 publications

Basal ganglia: physiological, behavioral, and computational studies

Basal ganglia: physiological, behavioral, and computational studies

Dopamine Selectively Modulates the Outcome of Learning Unnatural Action–Valence Associations

Slips of Action and Sequential Decisions: A Cross-Validation Study of Tasks Assessing Habitual and Goal-Directed Action Control

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