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.
Highlights
Newborn babies orient toward faces and schematic face-like figures
Based on the response areas with the largest response magnitudes in the visual field (VF), 146 neurons were divided into three groups: neurons with the largest response areas in the upper VF (SC neurons with upper receptive fields (RFs), n = 46), neurons with lower RFs (n = 68), and those with central RFs (n = 32; for definition of RF, see ‘‘Materials and Methods’’ section)
The upper VF, compared with the lower VF, has been suggested to be associated with visual search and object recognition (Previc, 1990), and saccadic latencies were shorter when static targets were presented in the upper VF (Heywood and Churcher, 1980). These findings suggest that the superior colliculus (SC) might be important to orient to faces in the upper VF
Summary
Newborn babies orient toward faces and schematic face-like figures (three filled circles on a bright ellipse; Johnson et al, 1991). Newly hatched chicks or chicks reared in dark, in which the optic tectum is the homolog of the mammal SC (Butler and Hodos, 2005), show preference for the similar schematic face-like figures and photos of human faces (Rosa-Salva et al, 2010, 2011). These behavioral data suggest that the vertebrate brain may have an innate face processing system or an innate prototypical face template (‘‘Conspec’’ Morton and Johnson, 1991)
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