Subjective feeling of control during fNIRS-based neurofeedback targeting the DL-PFC is related to neural activation determined with short-channel correction

PLOS ONE RESEARCH ARTICLE Subjective feeling of control during fNIRSbased neurofeedback targeting the DL-PFC is related to neural activation determined with short-channel correction Ambre Godet1☯, Yann Serrand1☯, Alexandra Fortier ID1, Brieuc Léger1, Elise Bannier2,3, David Val-Laillet ID1*, Nicolas Coquery ID1 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 INRAE, INSERM, Univ Rennes, CHU Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France, 2 Inria, CRNS, Inserm, IRISA UMR 6074, Empenn U1228, Univ Rennes, Rennes, France, 3 CHU Rennes, Radiology Department, Rennes, France ☯ These authors contributed equally to this work. * Abstract OPEN ACCESS Citation: Godet A, Serrand Y, Fortier A, Léger B, Bannier E, Val-Laillet D, et al. (2023) Subjective feeling of control during fNIRS-based neurofeedback targeting the DL-PFC is related to neural activation determined with short-channel correction. PLoS ONE 18(8): e0290005. https://doi. org/10.1371/journal.pone.0290005 Editor: Xiong Jiang, Georgetown University Medical Center, UNITED STATES Received: December 16, 2022 Accepted: July 31, 2023 Published: August 16, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0290005 Copyright: © 2023 Godet et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Raw data are available (https://doi.org/10.57745/XOAXC6). Neurofeedback (NF) training is a promising preventive and therapeutic approach for brain and behavioral impairments, the dorsolateral prefrontal cortex (DL-PFC) being a relevant region of interest. Functional near-infrared spectroscopy (NIRS) has recently been applied in NF training. However, this approach is highly sensitive to extra-cerebral vascularization, which could bias measurements of cortical activity. Here, we examined the feasibility of a NF training targeting the DL-PFC and its specificity by assessing the impact of physiological confounds on NF success via short-channel offline correction under different signal filtering conditions. We also explored whether the individual mental strategies affect the NF success. Thirty volunteers participated in a single 15-trial NF session in which they had to increase the oxy-hemoglobin (HbO2) level of their bilateral DL-PFC. We found that 0.01–0.09 Hz band-pass filtering was more suited than the 0.01–0.2 Hz band-pass filter to highlight brain activation restricted to the NF channels in the DL-PFC. Retaining the 10 out of 15 best trials, we found that 18 participants (60%) managed to control their DL-PFC. This number dropped to 13 (43%) with short-channel correction. Half of the participants reported a positive subjective feeling of control, and the “cheering” strategy appeared to be more effective in men (p<0.05). Our results showed successful DL-PFC fNIRS-NF in a single session and highlighted the value of accounting for extra cortical signals, which can profoundly affect the success and specificity of NF training. Introduction Neurofeedback (NF) is a neurocognitive procedure training aiming to assist people in learning to self-regulate their neural activity in a specific brain region [1]. With the help of neuroimaging techniques (e.g. electroencephalography–EEG, functional magnetic resonance imaging– fMRI, functional near-infrared spectroscopy–fNIRS), the activity of a specific brain area can be measured in real-time. During NF, an indicator of this brain activity can be presented to the PLOS ONE | https://doi.org/10.1371/journal.pone.0290005 August 16, 2023 1 / 17 PLOS ONE Funding: The present research was funded by the University of Rennes 1, Fondation de l’Avenir, the Benjamin Delessert Institute, and INRAE. A. Godet received a PhD grant from the University of Rennes 1. The fNIRS device used in this study was funded by CNRS INS2I and FEDER. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abbreviations: ADHD, attention deficit hyperactivity disorder; BOLD, blood oxygen level dependen; DL-PFC, dorsolateral prefrontal cortex; EEG, electroencephalography; fMRI, functional magnetic resonance imaging; fNIRS, functional near-infrared spectroscopy; GLM, generalized linear model; HbR, deoxy-hemoglobin; HbO2, oxyhemoglobin; HRF, hemodynamic response function; ROI, region of interest; SC, shortchannels. Neurofeedback targeting the DL-PFC participant as a metaphorical representation through a sensory modality (e.g. visual, auditory). The application of NF-based training protocols covers a wide range of research areas, from enhancing cognitive abilities in healthy individuals, to improving health conditions and behaviors in the context of neurocognitive disorders. The NIRS-based NF approach is an alternative to EEG and fMRI with great potential for translational research and clinical applications [2, 3]. As an optical brain imaging technique, fNIRS is less expensive and more accessible than fMRI, and less sensitive to movement artefacts compared to EEG, leading to a wider range of application in psychiatry and behavioral research among others [4, 5]. Although fNIRS displays lower temporal resolution as compared to EEG and lower spatial resolution as compared to fMRI (i. e. fNIRS acquisition signals are restricted to cortical areas), its use is increasing for NF studies due to its portability and low motion sensitivity. In particular, fNIRS-NF training protocols have been used to improve cognitive functions in elderly individuals [6], in impulsive adults [7], as well as in children and adults diagnosed with attention deficit hyperactivity disorder (ADHD) [8–10]. FNIRS-NF can also be applied to improve motor rehabilitation outcomes in stroke survivors [11]. Beyond specific pathologies, fNIRS-NF has been implemented to improve cognitive abilities (executive functioning), such as working memory [12], emotion regulation [13] and cognitive flexibility [14]. Greater brain activity requires increased oxygen consumption and higher cerebral blood flow. With NIRS, brain activity is measured indirectly by sending continuous light in red and in near infrared wavelengths to assess changes in oxy-hemoglobin (HbO2) and deoxy-hemoglobin (HbR) relative concentrations in human tissues [15, 16]. As compared to electrodes in EEG that acquire electrical brain activity, with fNIRS, optods (i.e. paired light sources and detectors), measure changes in oxygen concentration reflecti (...truncated)