Differential Contributions of Ventral Striatum Subregions to the Motivational and Hedonic Components of the Affective Processing of Reward

Pool, Eva; Tord, David Munoz; Delplanque, Sylvain; Stussi, Yoann; Cereghetti, Donato; Vuilleumier, Patrik; Sander, David

doi:10.1523/jneurosci.1124-21.2022

Cited by 20 publications

(14 citation statements)

References 67 publications

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“…In their discussion, Chan et al (2012) suggest that VS activation during humor comprehension might be related to a feeling of relief associated with incongruity resolution that might be separate from the amusement feeling of humor appreciation. The VS is also implicated in reward expectation ( Knutson et al, 2001 ; de la Fuente-Fernández et al, 2002 ; Filimon et al, 2020 ; Pool et al, 2022 ). Given that humor comprehension is an effortful process, activation of the VS in anticipation of a potential humor-appreciation-related reward might help to drive the humor comprehension process forward.…”

Section: Discussionmentioning

confidence: 99%

Establishing the Roles of the Dorsal and Ventral Striatum in Humor Comprehension and Appreciation with fMRI

Prenger,

Gilchrist,

Van Hedger

et al. 2023

J. Neurosci.

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Humor comprehension (i.e., getting a joke) and humor appreciation (i.e., enjoying a joke) are distinct, cognitively complex processes. Functional magnetic resonance imaging (fMRI) investigations have identified several key cortical regions but have overlooked subcortical structures that have theoretical importance in humor processing. The dorsal striatum (DS) contributes to working memory, ambiguity processing, and cognitive flexibility, cognitive functions that are required to accurately recognize humorous stimuli. The ventral striatum (VS) is critical in reward processing and enjoyment. We hypothesized that the DS and VS play important roles in humor comprehension and appreciation, respectively. We investigated the engagement of these regions in these distinct processes using fMRI. Twenty-six healthy young male and female human adults completed two humor-elicitation tasks during a 3 tesla fMRI scan consisting of a traditional behavior-based joke task and a naturalistic audiovisual sitcom paradigm (i.e.,Seinfeldviewing task). Across both humor-elicitation methods, whole-brain analyses revealed cortical activation in the inferior frontal gyrus, the middle frontal gyrus, and the middle temporal gyrus for humor comprehension, and the temporal cortex for humor appreciation. Additionally, with region of interest analyses, we specifically examined whether DS and VS activation correlated with these processes. Across both tasks, we demonstrated that humor comprehension implicates both the DS and the VS, whereas humor appreciation only engages the VS. These results establish the role of the DS in humor comprehension, which has been previously overlooked, and emphasize the role of the VS in humor processing more generally.SIGNIFICANCE STATEMENTHumorous stimuli are processed by the brain in at least two distinct stages. First, humor comprehension involves understanding humorous intent through cognitive and problem-solving mechanisms. Second, humor appreciation involves enjoyment, mirth, and laughter in response to a joke. The roles of smaller subcortical brain regions in humor processing, such as the DS and VS, have been overlooked in previous investigations. However, these regions are involved in functions that support humor comprehension (e.g., working memory ambiguity resolution, and cognitive flexibility) and humor appreciation (e.g., reward processing, pleasure, and enjoyment). In this study, we used neuroimaging to demonstrate that the DS and VS play important roles in humor comprehension and appreciation, respectively, across two different humor-elicitation tasks.

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Section: Discussionmentioning

confidence: 99%

Establishing the Roles of the Dorsal and Ventral Striatum in Humor Comprehension and Appreciation with fMRI

Prenger,

Gilchrist,

Van Hedger

et al. 2023

J. Neurosci.

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“…In neuroscience, recent evidence has specifically connected the ventral striatum as a key player in the transition mechanism of implicit to explicit memory formation in incidental learning. The ventral striatum is mainly associated to motivational and reward processes 49 releasing dopamine in rewarding situations, consequently enhancing the generation of explicit memory. In a study by Clos et al (2018) 10 , which also included a sequential task, the dopaminergic level was pharmacologically modulated in human adults.…”

Section: Discussionmentioning

confidence: 99%

Enriched environments enhance the development of explicit memory in an incidental learning task

Jaap

Maack

Taesler

et al. 2022

Sci Rep

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Learning, rendered in an implicit (unconscious) or explicit (conscious) way, is a crucial part of our daily life. Different factors, like attention or motivation, influence the transformation from implicit to explicit memory. Via virtual reality a lively and engaging surrounding can be created, whereby motivational processes are assumed to be a vital part of the transition from implicit to explicit memory. In the present study, we tested the impact of an enriched virtual reality compared to two conventional, non-enriched 2D-computer-screen based tasks on implicit to explicit memory transformation, using an audio-visual sequential association task. We hypothesized, that the immersive nature of the VR surrounding enhances the transfer from implicit to explicit memory. Notably, the overall amount of learned sequence pairs were not significantly different between experimental groups, but the degree of awareness was affected by the different settings. However, we observed an increased level of explicitly remembered pairs within the VR group compared to two screen-based groups. This finding clearly demonstrates that a near-natural experimental setting affects the transformation process from implicit to explicit memory.

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“…In order to assess whether affect explains variance beyond observable reward, initial investigations necessarily measure both. Future research may expand beyond this point of departure, using affect and its prediction errors to complement our understanding of valuation in contexts where value is less tangible than monetary reward ( Lindström et al, 2021 ; E. R. Pool et al, 2022 ; Tamir & Mitchell, 2012 ), encompassing policy decisions, social interactions, and more. The potential breadth of this approach is made evident in a recent study that ventured beyond tangible reward by leveraging affective prediction errors to study wishful thinking ( Melnikoff & Strohminger, 2023 ).…”

Section: Directions Aheadmentioning

confidence: 99%

Hidden Reward: Affect and Its Prediction Errors as Windows Into Subjective Value

Vollberg,

Sander

2024

Curr Dir Psychol Sci

Self Cite

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Scientists increasingly apply concepts from reinforcement learning to affect, but which concepts should apply? And what can their application reveal that we cannot know from directly observable states? An important reinforcement learning concept is the difference between reward expectations and outcomes. Such reward prediction errors have become foundational to research on adaptive behavior in humans, animals, and machines. Owing to historical focus on animal models and observable reward (e.g., food or money), however, relatively little attention has been paid to the fact that humans can additionally report correspondingly expected and experienced affect (e.g., feelings). Reflecting a broader “rise of affectivism,” attention has started to shift, revealing explanatory power of expected and experienced feelings—including prediction errors—above and beyond observable reward. We propose that applying concepts from reinforcement learning to affect holds promise for elucidating subjective value. Simultaneously, we urge scientists to test—rather than inherit—concepts that may not apply directly.

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Differential Contributions of Ventral Striatum Subregions to the Motivational and Hedonic Components of the Affective Processing of Reward

Abstract: Differential contributions of ventral striatum subregions to the motivational and hedonic components of the affective processing of reward Affective reward processes in the ventral striatum

Cited by 20 publications

References 67 publications

Establishing the Roles of the Dorsal and Ventral Striatum in Humor Comprehension and Appreciation with fMRI

Establishing the Roles of the Dorsal and Ventral Striatum in Humor Comprehension and Appreciation with fMRI

Enriched environments enhance the development of explicit memory in an incidental learning task

Hidden Reward: Affect and Its Prediction Errors as Windows Into Subjective Value

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