Face perception in humans and nonhuman primates is rapid and accurate []. In the human brain, a network of visual-processing regions is specialized for faces []. Although face processing is a priority of the primate visual system, face detection is not infallible. Face pareidolia is the compelling illusion of perceiving facial features on inanimate objects, such as the illusory face on the surface of the moon. Although face pareidolia is commonly experienced by humans, its presence in other species is unknown. Here we provide evidence for face pareidolia in a species known to possess a complex face-processing system []: the rhesus monkey (Macaca mulatta). In a visual preference task [], monkeys looked longer at photographs of objects that elicited face pareidolia in human observers than at photographs of similar objects that did not elicit illusory faces. Examination of eye movements revealed that monkeys fixated the illusory internal facial features in a pattern consistent with how they view photographs of faces []. Although the specialized response to faces observed in humans [] is often argued to be continuous across primates [], it was previously unclear whether face pareidolia arose from a uniquely human capacity. For example, pareidolia could be a product of the human aptitude for perceptual abstraction or result from frequent exposure to cartoons and illustrations that anthropomorphize inanimate objects. Instead, our results indicate that the perception of illusory facial features on inanimate objects is driven by a broadly tuned face-detection mechanism that we share with other species.

Face recognition systems in monkey and human: are they the same thing?.

Results and Discussion

Figure 1 Experimental Methods Show full caption (A) Examples of the three stimulus types used (from left to right: unfamiliar female monkeys, illusory faces, and non-face objects). The non-face objects were selected from the public domain on the basis that they matched the examples of illusory faces for object content. (B) The results of the human experiment. Here, the rows represent individual subject data (n = 10) and columns represent the 45 images comprising the stimulus set. Importantly, none of the non-face objects was rated as being “face-like” (>100) on a 200-point scale (M non-face objects = 5.24; SEM = 0.45). Two pairwise contrasts confirmed that the non-face objects had a significantly smaller average score than either the monkey faces (p < 0.01, η2 = 0.99) or illusory faces (p < 0.01, η2 = 0.99). (C) The trial procedure for the three conditions of interest in the monkey experiment. Each trial consisted of three time periods: fixation, free viewing, and reward after successful trial completion or time out after trial aborts. To evaluate whether rhesus monkeys perceive face pareidolia, we focused on naturally occurring examples of illusory faces, as judged by human observers. We collected 15 photographs from the public domain of inanimate objects (e.g., food, appliances, and tools) shown to promote the perception of illusory faces, together with 15 photographs of equivalent objects that were not perceived to contain an illusory face (e.g., Figure 1 A). We confirmed that independent human observers either perceived an illusory face or not in each stimulus by collecting behavioral ratings from ten naive observers of how “face-like” each image was ( Figure 1 B).

16 Johnson M.H.

Dziurawiec S.

Ellis H.

Morton J. Newborns’ preferential tracking of face-like stimuli and its subsequent decline. 17 Goren C.C.

Sarty M.

Wu P.Y. Visual following and pattern discrimination of face-like stimuli by newborn infants. 11 Sugita Y. Face perception in monkeys reared with no exposure to faces. 12 Gothard K.M.

Erickson C.A.

Amaral D.G. How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task?. 11 Sugita Y. Face perception in monkeys reared with no exposure to faces. 12 Gothard K.M.

Erickson C.A.

Amaral D.G. How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task?. 17 Goren C.C.

Sarty M.

Wu P.Y. Visual following and pattern discrimination of face-like stimuli by newborn infants. 13 Dal Monte O.

Costa V.D.

Noble P.L.

Murray E.A.

Averbeck B.B. Amygdala lesions in rhesus macaques decrease attention to threat. 18 Leonard T.K.

Blumenthal G.

Gothard K.M.

Hoffman K.L. How macaques view familiarity and gaze in conspecific faces. 19 Keating C.F.

Keating E.G. Visual scan patterns of rhesus monkeys viewing faces. We tested whether monkeys perceive illusory face structure in stimuli that elicited face pareidolia in humans using an established paradigm that has been successfully used to measure face detection in non-verbal subjects, including human infants [] and rhesus monkeys []. In a free-viewing visual preference task, we presented monkeys with pairs of stimuli and measured the time they spent looking at each stimulus. It is well established that humans and monkeys look longer at faces than at other stimuli []. Thus, if monkeys perceive illusory face structure in the same objects as humans, then they should spend longer looking at objects containing illusory faces than at similar objects that do not. A second dependent measure was the location of fixations on the experimental stimuli because both monkeys and humans [] make a disproportionate number of fixations on the internal features of real faces under free-viewing conditions. Thus, if monkeys perceive the illusory faces, their pattern of fixations should focus on the illusory “eye” and “mouth” regions of these images.

4 = 8.08, p < 0.01, η2 = 0.94) [ 11 Sugita Y. Face perception in monkeys reared with no exposure to faces. 12 Gothard K.M.

Erickson C.A.

Amaral D.G. How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task?. 4 = 10.23, p < 0.01, η2 = 0.96; see 4 = 5.52, p = 0.005, η2 = 0.88; see 20 Winters S.

Dubuc C.

Higham J.P. Perspectives: the looking time experimental paradigm in studies of animal visual perception and cognition. 21 Méary D.

Li Z.

Li W.

Guo K.

Pascalis O. Seeing two faces together: preference formation in humans and rhesus macaques. 22 Mendelson M.J.

Haith M.M.

Goldman-Rakic P.S. Face scanning and responsiveness to social cues in infant rhesus monkeys. Figure 2 Experimental Results Show full caption (A) Bar graph indicates the average proportion of time spent looking at stimuli as a function of condition (error bars = ±SEM). We found the expected advantage for monkey faces over objects, together with the hypothesized advantage for illusory faces over objects. We computed the average mean difference in each condition (monkey faces LT subtracted from illusory faces LT [I − M]; non-face objects LT subtracted from illusory faces LT [I − O]; non-face objects LT subtracted from monkey faces LT [M − O]) and performed a one-way repeated-measures ANOVA (p < 0.01, η p 2 = 0.86) to confirm that illusory face paired with monkey face trials elicited the smallest stimulus preference (paired t tests, two-tailed; [I − M] versus [I − O], p < 0.01, η2 = 0.97; [I − M] versus [M − O], p = 0.016, η2 = 0.80; [I − O] versus [M − O], p = 0.300 η2 = 0.24). (B) Bar graph demonstrating the distribution of first fixations in the three conditions of interest (the number of first fixations is expressed as a proportion of the total number of trials in each condition; error bars = ±SEM). An analysis of the first fixation data indicated that, in trials where monkey faces were presented with non-face objects, subjects fixated the monkey faces first and more often (p = 0.01, η2 = 0.92). There was a similar advantage for illusory faces over non-face objects (p = 0.01, η2 = 0.96). As with the LT data, this analysis also revealed a significant preference for illusory faces over monkey faces (p = 0.01, η2 = 0.92). See also Figure S1 We recorded the eye movements of five rhesus monkeys while they were presented with pairs of stimuli on a computer screen (for details, see STAR Methods ). The monkeys received a juice reward for maintaining fixation within the screen region containing the stimuli during each trial. Stimuli consisted of illusory faces, matched control objects, and monkey faces ( Figure 1 C). We presented each of the 45 stimuli an equal number of times in every possible pairing (the total number of trials was 1,980 per monkey). The behavioral measure looking time (LT) was expressed as the proportion of time that the animals spent exploring each visual stimulus compared with total presentation time (5 s). Consistent with previous work, subjects spent more time looking at monkey faces than at objects (mean difference = 0.31; t= 8.08, p < 0.01, η= 0.94) []. Importantly, the subjects also showed a looking preference for objects with illusory faces compared to matched objects without illusory faces (mean difference = 0.33; t= 10.23, p < 0.01, η= 0.96; see Figure 2 A). Interestingly, monkeys spent an even longer time looking at objects with illusory faces than at monkey faces (mean difference = 0.16; t= 5.52, p = 0.005, η= 0.88; see Figure 2 A), which may reflect either a response to the unusual and unexpected nature of the illusory faces [] or an aversion to maintaining prolonged fixation on the faces of conspecifics [], an effect frequently observed in rhesus monkeys, but not well understood []. An analysis of the first fixation data yielded the same pattern of results; the monkeys reliably directed their initial gaze toward objects containing an illusory face compared to either matched objects or monkey faces (see Figure 2 B). Together, the results reveal a clear viewing preference for stimuli that elicit the perception of illusory face structure in humans.

23 Hsiao J.H.

Cottrell G. Two fixations suffice in face recognition. 24 Barton J.J.

Radcliffe N.

Cherkasova M.V.

Edelman J.

Intriligator J.M. Information processing during face recognition: the effects of familiarity, inversion, and morphing on scanning fixations. 14 = 1.49, p = 0.16, η2 = 0.36; 14 = 8.74, p < 0.01, η2 = 0.95; illusory faces versus objects, t 14 = 7.24, p < 0.01, η2 = 0.93; Figure 3 Fixations Calibrated in Degrees of Visual Angle and Superimposed on Stimuli Show full caption (A) Average number of fixations (≥150 ms) in two-dimensional density plots (three examples from each stimulus type; top row, monkey faces; middle row, illusory faces; bottom row, non-face objects). Data were normalized to each subject’s maximum fixation count and then averaged across subjects before being smoothed and superimposed on the corresponding stimulus for illustration using MATLAB’s surf function with interpolated shading. Unsmoothed data for every stimulus, together with individual subject maps (before averaging), are available in the Figure S3 (B) The range of grand r values as a function of stimulus type. After vectorizing the normalized fixation count data for each subject, we cross-correlated across subjects. This process yielded ten r values that were then averaged together to yield a single “grand r value” per stimulus. The lower r values evident for the non-face objects reflect the greater variance among individual subjects. (C) Classifier performance as a function of subject; the classifier was trained with 93.33% of the data (i.e., 14 out of 15 illusory face/non-face pairs) and tested with the remaining content-matched pair. Chance performance is 50%. See also Figures S2 and S3 To further evaluate whether the monkeys’ looking preference for objects with illusory faces reflects an experience of pareidolia similar to our own, we examined their eye gaze patterns. We divided each stimulus into 121 equally sized square bins (1° in height and width) and tallied the distribution of fixations directed to each of the 45 stimuli across all trials. For each subject, we created a two-dimensional density plot, normalized to the maximum number of fixations, and averaged these across all five subjects ( Figure 3 A). The density plots highlight that monkeys frequently fixated the “eye” and “mouth” regions of both the monkey faces and the illusory faces, a finding consistent with human gaze behavior when viewing real faces []. The high density of fixations on these areas unambiguously distinguished the illusory faces from the matched object stimuli, which elicited more variable patterns of fixation (see Figure S2 for all stimulus maps). Further, the spatial distribution of fixations showed a higher stimulus-specific correlation across subjects for the monkey face and illusory face stimuli (t= 1.49, p = 0.16, η= 0.36; Figure 3 B) than for the matched objects (monkey faces versus objects, t= 8.74, p < 0.01, η= 0.95; illusory faces versus objects, t= 7.24, p < 0.01, η= 0.93; Figure 3 B).

Given the visible differences between the fixation patterns for illusory faces compared to matched objects (see Figure S3 for individual subject plots), we used machine learning classification to test whether we could systematically predict the presence of an illusory face in an object from the fixation maps. A linear support vector machine was trained using yoked leave-one-exemplar-out classification on the fixation maps for viewing objects with illusory faces versus matched objects. For every subject, the classifier was able to predict whether the subject was looking at an example of pareidolia or a content-matched object from the raw (un-normalized) fixation density maps ( Figure 3 C; mean accuracy = 86%, SD = 1.92%; all p values < 0.01). As the classifier was required to generalize to new exemplars not used in the training set, the results indicate that there was a consistent difference in the pattern of eye movements monkeys made toward illusory faces versus matched non-face objects.

3 Crouzet S.M.

Kirchner H.

Thorpe S.J. Fast saccades toward faces: face detection in just 100 ms. 14 Taubert J.

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Alais D. The role of holistic processing in face perception: evidence from the face inversion effect. 25 Tsao D.Y.

Livingstone M.S. Mechanisms of face perception. 26 Parr L.A.

Heintz M.

Pradhan G. Rhesus monkeys (Macaca mulatta) lack expertise in face processing. 27 Dahl C.D.

Rasch M.J.

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Adachi I. The face inversion effect in non-human primates revisited - an investigation in chimpanzees (Pan troglodytes). 28 Parr L.A.

Winslow J.T.

Hopkins W.D. Is the inversion effect in rhesus monkeys face-specific?. 29 Wright A.A.

Roberts W.A. Monkey and human face perception: inversion effects for human faces but not for monkey faces or scenes. 30 Parr L.A.

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Hancock P.J. The organization of conspecific face space in nonhuman primates. 31 Leopold D.A.

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Giese M.A. Norm-based face encoding by single neurons in the monkey inferotemporal cortex. 32 Taubert J.

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Parr L.A. A comparative study of face processing using scrambled faces. 33 Taubert J.

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Parr L.A. The composite face effect in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). 34 Taubert J.

Parr L.A. Visual expertise does not predict the composite effect across species: a comparison between spider (Ateles geoffroyi) and rhesus (Macaca mulatta) monkeys. 11 Sugita Y. Face perception in monkeys reared with no exposure to faces. 35 Pascalis O.

de Haan M.

Nelson C.A. Is face processing species-specific during the first year of life?. 11 Sugita Y. Face perception in monkeys reared with no exposure to faces. 36 Afraz S.R.

Kiani R.

Esteky H. Microstimulation of inferotemporal cortex influences face categorization. 37 Tomonaga M.

Imura T. Efficient search for a face by chimpanzees (Pan troglodytes). 38 Sadagopan S.

Zarco W.

Freiwald W.A. A causal relationship between face-patch activity and face-detection behavior. 39 Tomonaga M. Visual search for orientation of faces by a chimpanzee (Pan troglodytes): face-specific upright superiority and the role of facial configural properties. Collectively, our results provide strong evidence that rhesus monkeys spontaneously perceive illusory faces on inanimate objects. This observation raises the fundamental question of abstraction: what prompts the primate visual system to detect any particular object or pattern as a “face”? Face detection is arguably the most fundamental process of face perception, because the system needs to know a face is present before making subsequent social judgements []. Nonetheless, nearly all studies of face processing in nonhuman primates have focused on mechanisms of individual recognition, for example, providing demonstrations of the inversion effect [], normative coding [], holistic processing [], and perceptual narrowing []. The few studies that have explicitly examined face detection have primarily used photographs of “real” faces drawn from a set of tightly controlled human face stimuli [], thus minimizing the contribution of low-level visual features.

40 Hong K.

Chalup S.K.

King R.A.R. Affective visual perception using machine pareidolia of facial expressions. The novel approach in the present study is to specifically exploit the false positives that arise when low-level visual features are spuriously arranged in a face-like configuration. A key element of face pareidolia in human and nonhuman primates is sufficient tolerance to detect faces among stimuli whose other features are clearly incongruent with a real face (e.g., on the green surface of a vegetable). Unlike faces themselves, images that elicit pareidolia are notably variable in their visual features. Similar to humans, rhesus monkeys naturally detected faces among this varied set of images, with no experimental assumptions about the optimal face category (i.e., conspecifics or human faces) or the ideal non-face category for comparison. Notably, face detection algorithms in artificial visual systems trained on human and cartoon faces can similarly detect examples of face pareidolia as judged by human observers []. This is consistent with the idea that detection of illusory face structure in non-face objects, whether in a brain-based or computer-based system, requires a basic representation (or face template) that is broadly tuned to facial features with a high degree of tolerance for local visual properties.