A neuronal theta band signature of error monitoring during integration of facial expression cues

Camila Dias; Diana Costa; Teresa Sousa; João Castelhano; Verónica Figueiredo; Andreia C Pereira; Miguel Castelo-Branco

doi:10.7717/peerj.12627

A neuronal theta band signature of error monitoring during integration of facial expression cues

PeerJ. 2022 Feb 17:10:e12627. doi: 10.7717/peerj.12627. eCollection 2022.

Authors

Camila Dias^{1

2}, Diana Costa^{1

2}, Teresa Sousa^{1

2}, João Castelhano^{1

2}, Verónica Figueiredo^{1

2}, Andreia C Pereira^{1

2}, Miguel Castelo-Branco^{1

2

3}

Affiliations

¹ CIBIT - Coimbra Institute for Biomedical Imaging and Translational Research, University of Coimbra, Coimbra, Portugal.
² ICNAS - Institute for Nuclear Sciences Applied to Health, University of Coimbra, Coimbra, Portugal.
³ FMUC - Faculty of Medicine, University of Coimbra, Coimbra, Portugal.

Abstract

Error monitoring is the metacognitive process by which we are able to detect and signal our errors once a response has been made. Monitoring when the outcome of our actions deviates from the intended goal is crucial for behavior, learning, and the development of higher-order social skills. Here, we explored the neuronal substrates of error monitoring during the integration of facial expression cues using electroencephalography (EEG). Our goal was to investigate the signatures of error monitoring before and after a response execution dependent on the integration of facial cues. We followed the hypothesis of midfrontal theta as a robust neuronal marker of error monitoring since it has been consistently described as a mechanism to signal the need for cognitive control. Also, we hypothesized that EEG frequency-domain components might bring advantage to study error monitoring in complex scenarios as it carries information from locked and non-phase-locked signals. A challenging go/no-go saccadic paradigm was applied to elicit errors: integration of facial emotional signals and gaze direction was required to solve it. EEG data were acquired from twenty healthy participants and analyzed at the level of theta band activity during response preparation and execution. Although theta modulation has been consistently demonstrated during error monitoring, it is still unclear how early it starts to occur. We found theta power differences at midfrontal channels between correct and error trials. Theta was higher immediately after erroneous responses. Moreover, before response initiation we observed the opposite: lower theta preceding errors. These results suggest theta band activity not only as an index of error monitoring, which is needed to enhance cognitive control, but also as a requisite for success. This study adds to previous evidence for the role of theta band in error monitoring processes by revealing error-related patterns even before response execution in complex tasks, and using a paradigm requiring the integration of facial expression cues.

Keywords: EEG; Error monitoring; Eye tracking; Facial Cue integration; Theta oscillations.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Cues*
Electroencephalography
Emotions
Facial Expression
Humans
Theta Rhythm* / physiology

Grants and funding

This work was supported by FCT Portuguese national funding agency for science, research and technology [Grants BIGDATIMAGE, CENTRO-01-0145-FEDER-000016; BCI-CONNECT, PTDC/PSI-GER/30852/2017; B-RELIABLE, PTDC/EEI-AUT/30935/2017, DSAIPA/DS/0041/2020, PCIF/SSO/0082/2018, PAC -MEDPERSYST, POCI-01-0145-FEDER-016428, UI/BD/150832/2021]; and Bial Foundation [The neural circuitry underlying error monitoring during social cognition, 306/2018]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.