Striatal BOLD and midfrontal theta power express motivation for action

Algermissen, Johannes; Swart, Jennifer C.; Scheeringa, René; Cools, Roshan; Ouden, H.E.M. den

doi:10.1101/2020.09.11.292870

“…This idea is supported by a recent study in marmoset monkeys by Duan et al (2021) 65 showing that the rostral anterior cingulate cortex is necessary for detecting instrumental control of actions over outcomes, while the anterior orbitofrontal cortex (OFC) mediates Pavlovian influences on goal-directed behaviour. In line with this we have also recently shown that BOLD activity in the orbitofrontal / ventromedial prefrontal cortex predicts the degree of valence-induced invigoration 66 . This notion would align with previous work showing that modulating frontal dopamine can reconfigure connectivity patterns between OFC and other brain regions suggesting a key role in shaping functional brain circuitry 67 .…”

Section: Discussionsupporting

confidence: 83%

Cortical dopamine reduces the impact of motivational biases governing automated behaviour

Scholz

¹

,

Hook

²

,

Kandroodi

³

et al. 2021

Preprint

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Motivations shape our behaviour: the promise of reward invigorates, while in the face of punishment, we hold back. Abnormalities of motivational processing are implicated in clinical disorders characterised by excessive habits and loss of top-down control, notably substance and behavioural addictions. Striatal and frontal dopamine have been hypothesised to play complementary roles in the respective generation and control of these motivational biases. However, while dopaminergic interventions have indeed been found to modulate motivational biases, these previous pharmacological studies used regionally non-selective pharmacological agents. Here, we tested the hypothesis that frontal dopamine controls the balance between Pavlovian, bias-driven automated responding and instrumentally learned action values. Specifically, we examined whether selective enhancement of cortical dopamine either (i) enables adaptive suppression of Pavlovian control when biases are maladaptive; or (ii) non-specifically modulates the degree of bias-driven automated responding. Healthy individuals (n=35) received the catechol-o-methyltransferase (COMT) inhibitor tolcapone in a randomized, double-blind, placebo-controlled cross-over design, and completed a motivational Go NoGo task known to elicit motivational biases. In support of hypothesis (ii), tolcapone globally decreased motivational bias. Specifically, tolcapone improved performance on trials where the bias was unhelpful, but impaired performance in bias-congruent conditions. These results indicate a non-selective role for cortical dopamine in the regulation of motivational processes underpinning top-down control over automated behaviour. The findings have direct relevance to understanding neurobiological mechanisms underpinning addiction and obsessive-compulsive disorders, as well as highlighting a potential trans-diagnostic novel mechanism to address such symptoms.

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“…For combined EEG-fMRI analyses, we excluded the abovementioned six participants plus one more participant whose regression weights for every regressor were about ten times larger than for other participants, leaving 29 participants (M age = 23.00, 22 women). Exclusions were in line with a previous analysis of this data set (32). fMRI-and EEG-only results held when analyzing only those 29 participants (see S01).…”

Section: Participantssupporting

confidence: 84%

“…These filter settings allowed us to distinguish the delta, theta, alpha, and beta band, while filtering out residual high-frequency MR noise. This low-pass filter cut-off was different from a previous analysis of this data in which we set it at 15 Hz (32) because in this analysis, we had a hypothesis on outcome valence encoding in the beta range. We then applied linear baseline correction based on the 200 ms prior to cue onset and used ICA to detect and reject independent components related to eye-blinks, saccades, head motion, and residual MR artifacts (mean number of rejected components per participant: 32.694, range .…”

Section: Eeg Pre-processingmentioning

confidence: 98%

“…For the first purpose, we analyzed choice data (Go/ NoGo) using mixed-effects logistic regression that included factors required action (Go/ NoGo; note that this approach collapses across Go LEFT and Go RIGHT responses), cue valence (Win/ Avoid), and their interaction (also reported in) (32). Participants learned the task, i.e., they performed more Go responses towards Go than NoGo cues (main effect of required action: b = 0.815, SE = 0.113, χ 2 (1) = 32.008, p < .001).…”

Section: Regression Analyses Of Behaviormentioning

confidence: 99%

“…All analyses were performed on the average signal of a-priori selected channels Fz, FCz, and Cz based on (9,32). We again performed model-free and model-based analyses.…”

Section: Eeg Analysesmentioning

confidence: 99%

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Prefrontal signals precede striatal signals for biased credit assignment to (in)actions

Algermissen

¹

,

Swart

²

,

Scheeringa

³

et al. 2021

Preprint

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Actions are biased by the outcomes they can produce: Humans are more likely to show action under reward prospect, but hold back under punishment prospect. Such motivational biases derive not only from biased response selection, but also from biased learning: humans tend to attribute rewards to their own actions, but are reluctant to attribute punishments to having held back. The neural origin of these biases is unclear; in particular, it remains open whether motivational biases arise solely from an evolutionarily old, subcortical architecture or also due to younger, cortical influences. Simultaneous EEG-fMRI allowed us to track which regions encoded biased prediction errors in which order. Biased prediction errors occurred in cortical regions (ACC, vmPFC, PCC) before subcortical regions (striatum). These results highlight that biased learning is not a mere feature of the basal ganglia, but arises through prefrontal cortical contributions, revealing motivational biases to be a potentially flexible, sophisticated mechanism.

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Cortical dopamine reduces the impact of motivational biases governing automated behaviour

Scholz

¹

,

Hook

²

,

Kandroodi

³

et al. 2022

Neuropsychopharmacol.

Self Cite

View full text Add to dashboard Cite

Motivations shape our behaviour: the promise of reward invigorates, while in the face of punishment, we hold back. Abnormalities of motivational processing are implicated in clinical disorders characterised by excessive habits and loss of top-down control, notably substance and behavioural addictions. Striatal and frontal dopamine have been hypothesised to play complementary roles in the respective generation and control of these motivational biases. However, while dopaminergic interventions have indeed been found to modulate motivational biases, these previous pharmacological studies used regionally non-selective pharmacological agents. Here, we tested the hypothesis that frontal dopamine controls the balance between Pavlovian, bias-driven automated responding and instrumentally learned action values. Specifically, we examined whether selective enhancement of cortical dopamine either (i) enables adaptive suppression of Pavlovian control when biases are maladaptive; or (ii) non-specifically modulates the degree of bias-driven automated responding. Healthy individuals (n=35) received the catechol-o-methyltransferase (COMT) inhibitor tolcapone in a randomized, double-blind, placebo-controlled cross-over design, and completed a motivational Go NoGo task known to elicit motivational biases. In support of hypothesis (ii), tolcapone globally decreased motivational bias. Specifically, tolcapone improved performance on trials where the bias was unhelpful, but impaired performance in bias-congruent conditions. These results indicate a non-selective role for cortical dopamine in the regulation of motivational processes underpinning top-down control over automated behaviour. The findings have direct relevance to understanding neurobiological mechanisms underpinning addiction and obsessive-compulsive disorders, as well as highlighting a potential trans-diagnostic novel mechanism to address such symptoms.

show abstract

Striatal BOLD and midfrontal theta power express motivation for action

Cited by 7 publications

References 131 publications

Cortical dopamine reduces the impact of motivational biases governing automated behaviour

Cortical dopamine reduces the impact of motivational biases governing automated behaviour

Prefrontal signals precede striatal signals for biased credit assignment to (in)actions

Cortical dopamine reduces the impact of motivational biases governing automated behaviour

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