Easy to learn, hard to suppress: The impact of learned stimulus–outcome associations on subsequent action control

Wouwe, Nelleke C. van; Wildenberg, Wery P. M. van den; Ridderinkhof, K. Richard; Claassen, Daniel O.; Wylie, Scott A.

doi:10.1016/j.bandc.2015.10.007

Cited by 7 publications

(17 citation statements)

References 77 publications

(109 reference statements)

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“…In addition, both groups learned to withhold action to avoid punishment more effectively than to withhold action to gain reward. These patterns replicate previous studies using a similar paradigm in healthy adults (van Wouwe et al, 2015; Wagenbreth et al, 2015; Chowdhury, Guitart-Masip, Lambert, Dayan, et al, 2013; Chowdhury, Guitart-Masip, Lambert, Dolan, et al, 2013; Guitart-Masip, Chowdhury, et al, 2012; Guitart-Masip, Huys, et al, 2012). Our findings also replicate improved outcomes on learning to withhold to gain reward with DA as found in a levodopa study in HCs by Guitart-Masip et al (2014).…”

Section: Discussionsupporting

confidence: 89%

“…The action–valence paradigm also offers a novel tool for investigating the effects of pharmacologic and surgical interventions (e.g., deep brain stimulation) aimed at modulating BG activity selectively. We recently demonstrated that implicit processing of already formed natural and unnatural action–valence associations, even when irrelevant to a current task, produces dissociable effects on cognitive control mechanisms (van Wouwe et al, 2015). How established action–valence learning and biases interact with cognitive control mechanisms that are also linked to frontal BG circuits could provide new insight into a range of behavioral deficits involving poor control over strong urges and impulses.…”

Section: Discussionmentioning

confidence: 99%

“…Figure 1 depicts two example trials of the action–valence learning task (a similar design was used in van Wouwe et al, 2015). Participants were instructed that the goal of this task was to learn to act or withhold action to each of four color patches to maximize monetary earnings by gaining rewards and avoiding losses (i.e., punishments).…”

Section: Methodsmentioning

confidence: 99%

“…An emerging literature reveals that action control processes and reward/punishment learning processes, which are typically studied in isolation, are highly interactive (van Wouwe et al, 2015; Chowdhury, Guitart-Masip, Lambert, Dayan, et al, 2013; Chowdhury, Guitart-Masip, Lambert, Dolan, & Düzel, 2013; Guitart-Masip, Chowdhury, et al, 2012; Guitart-Masip, Huys, et al, 2012). Longstanding theories linking frontal BG circuitries, particularly dopamine (DA) modulation, to action selection and reinforcement learning mechanisms have elevated these networks as leading candidates for the integrative formation of stimulus–action–outcome associations (Aron et al, 2007; Bogacz & Gurney, 2007; McClure, Berns, & Montague, 2003; Schultz, 2002; Alexander, DeLong, & Strick, 1986).…”

Section: Introductionmentioning

confidence: 99%

“…A recent learning paradigm orthogonalizes action and outcome valence so that all combinations of learning to act or to withhold action to gain reward or to avoid punishment can be measured (see van Wouwe et al, 2015; Wagenbreth et al, 2015; Guitart-Masip, Chowdhury, et al, 2012; Guitart-Masip, Huys, et al, 2012). This paradigm confirms strong, natural learning biases such that action is more easily associated with reward and withholding action is more easily associated with punishment avoidance (Freeman, Alvernaz, Tonnesen, Linderman, & Aron, 2015; Wagenbreth et al, 2015; Freeman, Razhas, & Aron, 2014; Guitart-Masip, Chowdhury, et al, 2012; Guitart-Masip, Huys, et al, 2012; Everitt, Dickinson, & Robbins, 2001).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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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The human subthalamic nucleus and globus pallidus internus differentially encode reward during action control

Rossi

Peden

Castellanos

et al. 2017

Human Brain Mapping

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The subthalamic nucleus (STN) and globus pallidus internus (GPi) have recently been shown to encode reward, but few studies have been performed in humans. We investigated STN and GPi encoding of reward and loss (i.e., valence) in humans with Parkinson's disease. To test the hypothesis that STN and GPi neurons would change their firing rate in response to reward- and loss-related stimuli, we recorded the activity of individual neurons while participants performed a behavioral task. In the task, action choices were associated with potential rewarding, punitive, or neutral outcomes. We found that STN and GPi neurons encode valence-related information during action control, but the proportion of valence-responsive neurons was greater in the STN compared to the GPi. In the STN, reward-related stimuli mobilized a greater proportion of neurons than loss-related stimuli. We also found surprising limbic overlap with the sensorimotor regions in both the STN and GPi, and this overlap was greater than has been previously reported. These findings may help to explain alterations in limbic function that have been observed following deep brain stimulation therapy of the STN and GPi. Hum Brain Mapp 38:1952-1964, 2017. © 2017 Wiley Periodicals, Inc.

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The influence of associative reward learning on motor inhibition

Marchner

Preuschhof

2021

Psychological Research

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Stimuli that predict a rewarding outcome can cause difficulties to inhibit unfavourable behaviour. Research suggests that this is also the case for stimuli with a history of reward extending these effects on action control to situations, where reward is no longer accessible. We expand this line of research by investigating if previously reward-predictive stimuli promote behavioural activation and impair motor inhibition in a second unrelated task. In two experiments participants were trained to associate colours with a monetary reward or neutral feedback. Afterwards participants performed a cued go/no-go task, where cues appeared in the colours previously associated with feedback during training. In both experiments training resulted in faster responses in rewarded trials providing evidence of a value-driven response bias as long as reward was accessible. However, stimuli with a history of reward did not interfere with goal-directed action and inhibition in a subsequent task after removal of the reward incentives. While the first experiment was not conclusive regarding an impact of reward-associated cues on response inhibition, the second experiment, validated by Bayesian statistics, clearly questioned an effect of reward history on inhibitory control. This stands in contrast to earlier findings suggesting that the effect of reward history on subsequent action control is not as consistent as previously assumed. Our results show that participants are able to overcome influences from Pavlovian learning in a simple inhibition task. We discuss our findings with respect to features of the experimental design which may help or complicate overcoming behavioural biases induced by reward history.

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Easy to learn, hard to suppress: The impact of learned stimulus–outcome associations on subsequent action control

Cited by 7 publications

References 77 publications

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

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

The human subthalamic nucleus and globus pallidus internus differentially encode reward during action control

The influence of associative reward learning on motor inhibition

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