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

Maimu Alissa Rehbein; Thomas Kroker; Constantin Winker; Lena Ziehfreund; Anna Reschke; Jens Bölte; Miroslaw Wyczesany; Kati Roesmann; Ida Wessing; Markus Junghöfer

doi:10.3389/fnins.2023.1219029

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

Front Neurosci. 2023 Aug 15:17:1219029. doi: 10.3389/fnins.2023.1219029. eCollection 2023.

Authors

Maimu Alissa Rehbein^#^{1

2}, Thomas Kroker^#^{1

2}, Constantin Winker^{1

2}, Lena Ziehfreund¹, Anna Reschke¹, Jens Bölte^{2

3}, Miroslaw Wyczesany⁴, Kati Roesmann^{1

2

5}, Ida Wessing^{1

2

6}, Markus Junghöfer^{1

2}

Affiliations

¹ Institute for Biomagnetism and Biosignalanalysis, University Hospital Münster, Münster, Germany.
² Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Münster, Münster, Germany.
³ Institute of Psychology, University of Münster, Münster, Germany.
⁴ Institute of Psychology, Jagiellonian University, Kraków, Poland.
⁵ Institute for Clinical Psychology, University of Siegen, Siegen, Germany.
⁶ Department of Child and Adolescent Psychiatry, University Hospital Münster, Münster, Germany.

^# Contributed equally.

Abstract

Introduction: Studies 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).

Methods: Participants 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.

Results: Regarding 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.

Discussion: Our 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.

Keywords: magnetoencephalography; prediction error; reward prediction; reward processing; transcranial direct current stimulation; ventromedial prefrontal cortex.

Grants and funding

This study was funded by the DFG (project JU 445/9-1), by the Interdisciplinary Center for Clinical Research of the University of Münster (Ju2/024/15), and by the Polish National Science Center (UMO-2018/31/G/HS6/02490).