Dissociation between Active and Observational Learning from Positive and Negative Feedback in Parkinsonism

Stefan Kobza,Stefano Ferrea,Christian Bellebaum,Bettina Pollok,Alfons Schnitzler,Martin Südmeyer,Sonia Brucki

doi:10.1371/journal.pone.0050250

Stefan Kobza, Stefano Ferrea + Show 5 more

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https://doi.org/10.1371/journal.pone.0050250

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Abstract

Feedback to both actively performed and observed behaviour allows adaptation of future actions. Positive feedback leads to increased activity of dopamine neurons in the substantia nigra, whereas dopamine neuron activity is decreased following negative feedback. Dopamine level reduction in unmedicated Parkinson’s Disease patients has been shown to lead to a negative learning bias, i.e. enhanced learning from negative feedback. Recent findings suggest that the neural mechanisms of active and observational learning from feedback might differ, with the striatum playing a less prominent role in observational learning. Therefore, it was hypothesized that unmedicated Parkinson’s Disease patients would show a negative learning bias only in active but not in observational learning. In a between-group design, 19 Parkinson’s Disease patients and 40 healthy controls engaged in either an active or an observational probabilistic feedback-learning task. For both tasks, transfer phases aimed to assess the bias to learn better from positive or negative feedback. As expected, actively learning patients showed a negative learning bias, whereas controls learned better from positive feedback. In contrast, no difference between patients and controls emerged for observational learning, with both groups showing better learning from positive feedback. These findings add to neural models of reinforcement-learning by suggesting that dopamine-modulated input to the striatum plays a minor role in observational learning from feedback. Future research will have to elucidate the specific neural underpinnings of observational learning.

Highlights

Humans are constantly confronted with situations in which a choice between different actions is required
In line with a recent study by Shiner and colleagues [32], who showed learning of stimulusoutcome contingencies independent from dopaminergic drug state (ON vs. OFF) in Parkinson’s Disease (PD) patients, learning of contingencies was comparable between unmedicated PD patients and healthy controls for both the observational and the active learning task in the present study
A bias to learn better from negative feedback was only present in actively learning PD patients OFF medication, whereas patients who learned by observation showed the same behavioural pattern as healthy controls, who learned better from positive feedback across tasks

Summary

Introduction

Humans are constantly confronted with situations in which a choice between different actions is required. Decisions can be optimised by learning from the consequences of the chosen actions. Positive consequences, such as reward or positive feedback, increase the frequency of behaviour, whereas actions leading to negative consequences, e.g. punishment or negative feedback, are less likely to reoccur. DA neurons of the substantia nigra (SN) are connected with the striatum [6] and the frontal cortex [7]. Functional neuroimaging studies in humans consistently revealed reward-related activations in the striatum and the anterior cingulate cortex (ACC) The ventral striatum including the nucleus accumbens has been shown to code a reward prediction error during the processing of reward stimuli The ventral striatum including the nucleus accumbens has been shown to code a reward prediction error during the processing of reward stimuli (e.g. [11,14,15,16])

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