How the brain differentiates human and monkey faces: Neuromagnetic evidence from spatiotemporal dynamics

Emi Yamada; Akinori Takeda; Hisato Nakazono; Mutsuhide Tanaka; Katsuya Ogata; Shozo Tobimatsu

doi:10.1016/j.neuroscience.2024.11.018

How the brain differentiates human and monkey faces: Neuromagnetic evidence from spatiotemporal dynamics

Neuroscience. 2024 Nov 16:565:80-90. doi: 10.1016/j.neuroscience.2024.11.018. Online ahead of print.

Authors

Emi Yamada¹, Akinori Takeda², Hisato Nakazono³, Mutsuhide Tanaka⁴, Katsuya Ogata⁵, Shozo Tobimatsu⁶

Affiliations

¹ Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Department of Linguistics, Faculty of Humanities, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, Japan. Electronic address: e.yamada@kyudai.jp.
² Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Research Center for Brain Communication, Research Institute, Kochi University of Technology, 185 Miyanokuchi, Tosayamada, Kami City, Kochi 782-8502, Japan.
³ Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Department of Occupational Therapy, Faculty of Medical Science, Fukuoka International University of Health and Welfare, 3-6-40 Momochihama, Sawara-ku, Fukuoka 814-0001, Japan.
⁴ Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Department of Health and Welfare Occupational Therapy Course, Faculty of Health and Welfare, Prefectural University of Hiroshima, 1-1 Gakuen-cho, Mihara City, Hiroshima 723-0053, Japan.
⁵ Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Department of Speech and Hearing Sciences, School of Health Sciences at Fukuoka, International University of Health and Welfare, 137-1 Enokizu, Okawa, Fukuoka 831-8501, Japan.
⁶ Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan; Department of Orthoptics, Faculty of Medicine, Fukuoka International University of Health and Welfare, 3-6-40 Momochihama, Sawara-ku, Fukuoka 814-0001, Japan.

PMID: 39557190
DOI: 10.1016/j.neuroscience.2024.11.018

Abstract

Face recognition is an important aspect of human non-verbal communication. Event-related potentials or magnetic fields, such as the N170/M170 component, are considered essential neural markers of face processing. Compared to upright human faces, inverted human faces and upright but not inverted animal faces cause longer latencies and larger amplitudes of these components. However, the mechanisms underlying this factor remain unclear. To elucidate the spatiotemporal dynamics of the processing of inverted human and animal faces, we recorded face-selective responses (M170) to upright and inverted human and monkey faces using a 306-channel whole-head magnetoencephalography. Sensor analysis showed an increased M170 latency and amplitude for inverted human and upright animal faces. However, in the source analysis, the observed modulations of the estimated spatiotemporal dynamics were different from the sensor results: irrespective of species, upright faces activated wider areas in the ventral and dorsal visual regions compared with inverted faces. Additionally, face orientation differentially modulated the anterior region of the fusiform gyrus (FG) in both face categories. These results suggest that spatiotemporal dynamics differ in face orientation regardless of category and that the FG contributes little or nothing to the M170 modulation recorded in the scalp sensor. Furthermore, we demonstrated that inverted human and animal faces are processed via different mechanisms.

Keywords: Animal face; Anterior region of FG; Face inversion effect; Human face; M170; Magnetoencephalography.