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      A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

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          Abstract

          Human babies respond preferentially to faces or face-like images. It has been proposed that an innate and rapid face detection system is present at birth before the cortical visual pathway is developed in many species, including primates. However, in primates, the visual area responsible for this process is yet to be unraveled. We hypothesized that the superior colliculus (SC) that receives direct and indirect retinal visual inputs may serve as an innate rapid face-detection system in primates. To test this hypothesis, we examined the responsiveness of monkey SC neurons to first-order information of faces required for face detection (basic spatial layout of facial features including eyes, nose, and mouth), by analyzing neuronal responses to line drawing images of: (1) face-like patterns with contours and properly placed facial features; (2) non-face patterns including face contours only; and (3) nonface random patterns with contours and randomly placed face features. Here, we show that SC neurons respond stronger and faster to upright and inverted face-like patterns compared to the responses to nonface patterns, regardless of contrast polarity and contour shapes. Furthermore, SC neurons with central receptive fields (RFs) were more selective to face-like patterns. In addition, the population activity of SC neurons with central RFs can discriminate face-like patterns from nonface patterns as early as 50 ms after the stimulus onset. Our results provide strong neurophysiological evidence for the involvement of the primate SC in face detection and suggest the existence of a broadly tuned template for face detection in the subcortical visual pathway.

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          Most cited references 74

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          The many faces of configural processing.

          Adults' expertise in recognizing faces has been attributed to configural processing. We distinguish three types of configural processing: detecting the first-order relations that define faces (i.e. two eyes above a nose and mouth), holistic processing (glueing the features together into a gestalt), and processing second-order relations (i.e. the spacing among features). We provide evidence for their separability based on behavioral marker tasks, their sensitivity to experimental manipulations, and their patterns of development. We note that inversion affects each type of configural processing, not just sensitivity to second-order relations, and we review evidence on whether configural processing is unique to faces.
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            Neural bases of the non-conscious perception of emotional signals.

            Many emotional stimuli are processed without being consciously perceived. Recent evidence indicates that subcortical structures have a substantial role in this processing. These structures are part of a phylogenetically ancient pathway that has specific functional properties and that interacts with cortical processes. There is now increasing evidence that non-consciously perceived emotional stimuli induce distinct neurophysiological changes and influence behaviour towards the consciously perceived world. Understanding the neural bases of the non-conscious perception of emotional signals will clarify the phylogenetic continuity of emotion systems across species and the integration of cortical and subcortical activity in the human brain.
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              Center-periphery organization of human object areas.

              The organizing principles that govern the layout of human object-related areas are largely unknown. Here we propose a new organizing principle in which object representations are arranged according to a central versus peripheral visual field bias. The proposal is based on the finding that building-related regions overlap periphery-biased visual field representations, whereas face-related regions are associated with center-biased representations. Furthermore, the eccentricity maps encompass essentially the entire extent of object-related occipito-temporal cortex, indicating that most object representations are organized with respect to retinal eccentricity. A control experiment ruled out the possibility that the results are due exclusively to unequal feature distribution in these images. We hypothesize that brain regions representing object categories that rely on detailed central scrutiny (such as faces) are more strongly associated with processing of central information, compared to representations of objects that may be recognized by more peripheral information (such as buildings or scenes).
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                Author and article information

                Contributors
                Journal
                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                1662-5137
                06 February 2020
                2020
                : 14
                Affiliations
                1System Emotional Science, Faculty of Medicine, University of Toyama , Toyama, Japan
                2Primate Center and Laboratory of Neurosciences and Behavior, Department of Physiological Sciences, Institute of Biology, University of Brasília , Brasilia, Brazil
                3Laboratory of Neuroscience and Behavior, CEUMA University , São Luis, Brazil
                Author notes

                Edited by: Alessandra Angelucci, The University of Utah, United States

                Reviewed by: Ziad M. Hafed, University of Tübingen, Germany; Ludise Malkova, Georgetown University, United States

                *Correspondence: Hisao Nishijo nishijo@ 123456med.u-toyama.ac.jp

                These authors have contributed equally to this work

                Article
                10.3389/fnsys.2020.00005
                7025518
                Copyright © 2020 Le, Le, Nishimaru, Matsumoto, Takamura, Hori, Maior, Tomaz, Ono and Nishijo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 90, Pages: 16, Words: 10719
                Funding
                Funded by: Japan Society for the Promotion of Science 10.13039/501100001691
                Award ID: 16H04652
                Categories
                Neuroscience
                Original Research

                Neurosciences

                innate recognition, face detection, face features, superior colliculus, monkey

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