Effects of familiarity on child brain networks when listening to a storybook reading: A magneto-encephalographic study
Chiaki Hasegawa,
Tetsuya Takahashi,
Takashi Ikeda,
Yuko Yoshimura,
Hirotoshi Hiraishi,
Sou Nobukawa,
Daisuke N. Saito,
Hirokazu Kumazaki,
Ken Yaoi,
Masayuki Hirata,
Minoru Asada,
Mitsuru Kikuchi
Affiliations
Chiaki Hasegawa
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; JSPS Oversea Research Fellow RRA, Visiting Fellow, Department of Cognitive Science, Macquarie University, Tokyo 102-0083, Japan
Tetsuya Takahashi
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; Uozu Shinkei Sanatorium, Uozu 937-0017, Japan; Department of Neuropsychiatry, University of Fukui, Fukui 910-1193, Japan; Corresponding author.
Takashi Ikeda
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University, and University of Fukui, Osaka/Kanazawa/Hamamatsu/Chiba/Fukui, Japan
Yuko Yoshimura
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University, and University of Fukui, Osaka/Kanazawa/Hamamatsu/Chiba/Fukui, Japan; Institute of Human and Social Sciences, Kanazawa University, Kanazawa 921-1192, Japan
Hirotoshi Hiraishi
Department of Biofunctional Imaging, Preeminent Medical Photonics Education & Research Center, Hamamatsu University School of Medicine, Hamamatsu 431-3192, Japan
Sou Nobukawa
Department of Computer Science, Chiba Institute of Technology, Narashino 275-0016, Japan
Daisuke N. Saito
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University, and University of Fukui, Osaka/Kanazawa/Hamamatsu/Chiba/Fukui, Japan; Department of Psychology, Faculty of Psychology, Yasuda Woman's University, Hiroshima 731-0153, Japan
Hirokazu Kumazaki
National Institute of Mental Health, National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi, Kodaira, Tokyo 187-8553, Japan
Ken Yaoi
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University, and University of Fukui, Osaka/Kanazawa/Hamamatsu/Chiba/Fukui, Japan
Masayuki Hirata
Department of Neurological Diagnosis and Restoration, Osaka University Graduate School of Medicine, Suita 565-0871, Japan; Endowed Research Department of Clinical Neuroengineering Global Center for Medical Engineering and Informatics, Osaka University, Suita 565-0871, Japan
Minoru Asada
International Professional University of Technology in Osaka, Kita-ku 530-0001, Japan; Symbiotic Intelligent System Research Center, Institute for Open and Transdisciplinary Research Initiatives, Osaka University, Suita 565-0871, Japan
Mitsuru Kikuchi
Research Center for Child Mental Development, Kanazawa University, Kanazawa 920-8640, Japan; United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University, and University of Fukui, Osaka/Kanazawa/Hamamatsu/Chiba/Fukui, Japan; Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa 920-8641, Japan
Parent-child book reading is important for fostering the development of various lifelong cognitive and social abilities in young children. Despite numerous reports describing the effects of familiarity on shared reading for children, the exact neural basis of the functional network architecture remains unclear. We conducted Magnet-Encephalographic (MEG) experiments using graph theory to elucidate the role of familiarity in shared reading in a child's brain network and to measure the connectivity dynamics of a child while Listening to Storybook Reading (LSBR), which represents the daily activity of shared book reading between the child and caregiver. The LSBR task was performed with normally developing preschool- and school-age children (N = 15) under two conditions: reading by their own mother (familiar condition) vs. an experimenter (unfamiliar condition). We used the phase lag index (PLI), which captures synchronization of MEG signals, to estimate functional connectivity. For the whole brain network topology, an undirected weighted graph was produced using 68 brain regions as nodes and interregional PLI values as edges for five frequency bands. Behavioral data (i.e., the degree of attention and facial expressions) were evaluated from video images of the child's face during the two conditions. Our results showed enhanced widespread functional connectivity in the alpha band during the mother condition. In the mother condition, the whole brain network in the alpha band exhibited topographically high local segregation with high global integration, indicating an increased small-world property. Results of the behavioral analysis revealed that children were more attentive and showed more positive facial expressions in the mother condition than in the experimenter condition. Behavioral data were significantly correlated with graph metrics in the mother condition but not in the experimenter condition. In this study, we identified the neural correlates of a familiarity effect in children's brain connectivity dynamics during LSBR. Furthermore, these familiarity-related brain dynamics were closely linked to the child's behavior. Graph theory applied to MEG data may provide useful insight into the familiarity-related child brain response in a naturalistic setting and its relevance to child attitudes.
