Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing

Abstract

IntroductionStudies suggest an involvement of the ventromedial prefrontal cortex (vmPFC) in reward prediction and processing, with reward-based learning relying on neural activity in response to unpredicted rewards or non-rewards (reward prediction error, RPE). Here, we investigated the causal role of the vmPFC in reward prediction, processing, and RPE signaling by transiently modulating vmPFC excitability using transcranial Direct Current Stimulation (tDCS).MethodsParticipants received excitatory or inhibitory tDCS of the vmPFC before completing a gambling task, in which cues signaled varying reward probabilities and symbols provided feedback on monetary gain or loss. We collected self-reported and evaluative data on reward prediction and processing. In addition, cue-locked and feedback-locked neural activity via magnetoencephalography (MEG) and pupil diameter using eye-tracking were recorded.ResultsRegarding reward prediction (cue-locked analysis), vmPFC excitation (versus inhibition) resulted in increased prefrontal activation preceding loss predictions, increased pupil dilations, and tentatively more optimistic reward predictions. Regarding reward processing (feedback-locked analysis), vmPFC excitation (versus inhibition) resulted in increased pleasantness, increased vmPFC activation, especially for unpredicted gains (i.e., gain RPEs), decreased perseveration in choice behavior after negative feedback, and increased pupil dilations.DiscussionOur results support the pivotal role of the vmPFC in reward prediction and processing. Furthermore, they suggest that transient vmPFC excitation via tDCS induces a positive bias into the reward system that leads to enhanced anticipation and appraisal of positive outcomes and improves reward-based learning, as indicated by greater behavioral flexibility after losses and unpredicted outcomes, which can be seen as an improved reaction to the received feedback.

Higher‐order comparative reward processing is affected by noninvasive stimulation of the ventromedial prefrontal cortex

“…Behaviorally, we hypothesized that we would observe increased risk taking behavior (indicating increased reward approach and/or attenuated loss/risk aversion) after excitatory compared to inhibitory vmPFC stimulation, predominately reflecting the reward‐related function of the vmPFC (Knutson et al, 2003; Proudfit, 2015). This hypothesis can also be derived from previous findings of our group, as we observed higher reward expectancy after vmPFC excitation compared to inhibition (Rehbein et al, 2023). Thus, if the reward expectancy is increased, one should be more willing to gamble (i.e., to risk the gamble) for a higher amount of money.…”

“…Losses were rated as less pleasant while gains were rated as more pleasant after excitatory compared to inhibitory stimulation as indicated by post‐hoc t ‐tests. This analysis regarding the modulation of basic reward processing was implied by our previous study (Rehbein et al, 2023) and is thus a confirmatory, replication‐driven approach. (b) Change of the choice option (left vs. right choice option) as a function of stimulation and the actual outcome of the preceding trial analyzed with a mixed‐effects logistic regression.…”

“…Post‐hoc analyses were conducted using chi‐squared tests. This analysis regarding the expectancy of a greater reward after excitatory versus inhibitory stimulation was implied by our previous study (Rehbein et al, 2023) and is thus a confirmatory, replication‐driven approach. Box plots indicate means (black dot), medians (gray line), and lower and upper quartiles.…”

“…Finite element‐based forward modeling of tDCS currents has revealed that this electrode positioning induces maximal stimulation of the anterior vmPFC and minimal stimulation of other brain regions (Wagner et al, 2014). For the stimulation, a DC Stimulator Plus (NeuroConn GmbH, Ilmenau, Germany) was used, and it applied a maximum current of 1.5 mA for 10 min with fade‐in and fade‐out phases of 10 s. This stimulation intensity and duration proved to be effective in evoking behavioral as well as neural effects of stimulation in our previous studies on emotion perception (Junghofer et al, 2017; Winker et al, 2018, 2019, 2020), reward processing (Kroker et al, 2022; Rehbein et al, 2023) as well as fear generalization (Roesmann et al, 2021). While anodal stimulation depolarizes the membrane potential of underlying neurons and increases their excitability, a cathodal stimulation hyperpolarizes the membrane potential and diminishes the neurons' excitability (Sparing & Mottaghy, 2008).…”

“…Furthermore, we showed that excitatory vmPFC tDCS resulted in less biased and, thus, more rational decision‐making and feedback processing compared to inhibitory stimulation (Kroker et al, 2022). Although in the preceding financial gambling studies we tested stimulation‐driven modulations of rather basic gain versus loss processing (Kroker et al, 2022a, 2022b; Rehbein et al, 2023), it has been proposed that the vmPFC is also involved in higher‐order reward processing (e.g., Hiser & Koenigs, 2018). Therefore, in the present study, we aimed to investigate whether vmPFC tDCS affects more complex or higher‐order feedback evaluation in addition to modulating basic gain versus loss processing.…”