Association between eating behavior and the immediate neural activity caused by viewing food images presented in and out of awareness: A magnetoencephalography study

PLOS ONE RESEARCH ARTICLE Association between eating behavior and the immediate neural activity caused by viewing food images presented in and out of awareness: A magnetoencephalography study Rika Ishida, Akira Ishii ID*, Takashi Matsuo, Takayuki Minami, Takahiro Yoshikawa a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 Department of Sports Medicine, Osaka City University Graduate School of Medicine, Osaka, Japan * Abstract OPEN ACCESS Citation: Ishida R, Ishii A, Matsuo T, Minami T, Yoshikawa T (2022) Association between eating behavior and the immediate neural activity caused by viewing food images presented in and out of awareness: A magnetoencephalography study. PLoS ONE 17(12): e0275959. https://doi.org/ 10.1371/journal.pone.0275959 Editor: Zhishun Wang, Columbia University, UNITED STATES Received: September 28, 2020 Accepted: September 27, 2022 Published: December 29, 2022 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.0275959 Copyright: © 2022 Ishida 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: The Ethics Committee of Osaka City University which approved the protocol of our present study does Obesity is a serious health problem in modern society. Considering the fact that the outcomes of treatments targeting appetitive behavior are suboptimal, one potential reason proposed for these poor outcomes is that appetitive behavior is driven more by unconscious decision-making processes than by the conscious ones targeted by traditional behavioral treatments. In this study, we aimed to investigate both the conscious and unconscious decision-making processes related to eating behavior, and to examine whether an interaction related to eating behavior exists between conscious and unconscious neural processes. The study was conducted on healthy male volunteers who viewed pictures of food and nonfood items presented both above and below the awareness threshold. The oscillatory brain activity affected by viewing the pictures was assessed by magnetoencephalography. A visual backward masking procedure was used to present the pictures out of awareness. Neural activity corresponding to the interactions between sessions (i.e., food or non-food) and conditions (i.e., visible or invisible) was observed in left Brodmann’s areas 45 and 47 in the high-gamma (60–200 Hz) frequency range. The interactions were associated with eating behavior indices such as emotional eating and cognitive restraint, suggesting that conscious and unconscious neural processes are differently involved in eating behavior. These findings provide valuable clues for devising methods to assess conscious and unconscious appetite regulation in individuals with normal or abnormal eating behavior. Introduction Obesity is a serious health problem in modern society: The prevalence of overweight individuals and obesity are increasing worldwide [1]. Overweight and obesity cause a wide variety of health problems, including type 2 diabetes, dyslipidemia, hypertension, coronary heart disease, and certain kinds of cancer, such as colon cancer [2–4], which has a major effect on the PLOS ONE | https://doi.org/10.1371/journal.pone.0275959 December 29, 2022 1 / 17 PLOS ONE not allow public sharing of the raw MEG and MRI data since the data contain potentially sensitive information. The values behind the means and standard deviations, which are used to build figures, and the code for experimental task can be received by e-mail upon reasonable request. Nonauthor point of contact: The Ethics Committee of Osaka City University (. jp). Funding: "AI: JSPS KAKENHI Grant No. 16H03248 and TY: JSPS KAKENHI Grant No. 22K11732". Competing interests: The authors have declared that no competing interests exist. Eating behavior and conscious and unconscious neural responses to food increasing costs of medical care [5–7]. Since body weight depends on the balance between energy expenditure and food intake, behaviors related to food intake are important intervention targets to prevent obesity. It is estimated that even less than 0.5% of caloric intake over energy expenditure can lead to weight gain [8, 9]. Educational and/or behavioral interventions for addressing obesity are partially successful, with nearly half of treated patients returning to pre-treatment weights within 5 years of intervention completion [10–13]. Considering that the outcomes of treatments targeting appetitive behavior are suboptimal, one potential reason for these poor outcomes is that appetitive behavior is driven more by unconscious decision-making processes than by the conscious decisionmaking processes targeted by traditional behavioral treatments [14]. In fact, it has been demonstrated that the greater saliva production and the increased rating of hunger were caused by coupling the food-related stimuli presented below the threshold of awareness with positively valenced terms, suggesting that the unconscious processes, which would not evoke eatingrelated deliberation, can effectively modulate affective and motivational responses caused by food-related stimuli [15, 16]. It has also been reported that neural responses to visual food stimuli reflect some aspects of eating behaviors, and the neural mechanisms related to eating behaviors have been investigated based on neural responses to visual food stimuli [17]. In most of these studies, the visual food stimuli were presented above the threshold of awareness. However, it is of note that there has been a study in which the neural response to visual food stimuli presented below the threshold of awareness was examined using magnetoencephalography (MEG). Visual food stimuli were presented below the threshold of awareness using a backward masking procedure in their study, and the alterations in autonomic nervous activity and the neural response caused by the presentation of the stimuli were examined. Compared with a condition in which mosaic pictures created from original food stimuli were presented so as not to be recognized by the participants, the food stimuli presented so as not to be recognized by them caused the activation of sympathetic nervous activity and alterations in neural activity in Brodmann’s areas (BA) 47 and 13, which are related to the alteration of sympathetic nervous activity and the level of cognitive restraint of food intake, respectively [18]. These findings suggest the existence of unconscious processes related to eating behavior. The approach applied in the study that presenting visual (...truncated)