Inactivation of face-selective neurons alters eye movements when free viewing faces.

During free viewing, faces attract gaze and induce specific fixation patterns corresponding to the facial features. This suggests that neurons encoding the facial features are in the causal chain that steers the eyes. However, there is no physiological evidence to support a mechanistic link between face-encoding neurons in high-level visual areas and the oculomotor system. In this study, we targeted the middle face patches of the inferior temporal (IT) cortex in two macaque monkeys using an functional magnetic resonance imaging (fMRI) localizer. We then utilized muscimol microinjection to unilaterally suppress IT neural activity inside and outside the face patches and recorded eye movements while the animals free viewing natural scenes. Inactivation of the face-selective neurons altered the pattern of eye movements on faces: The monkeys found faces in the scene but neglected the eye contralateral to the inactivation hemisphere. These findings reveal the causal contribution of the high-level visual cortex in eye movements.

Beyond faces: the contribution of the amygdala to visual processing in the macaque brain.

The amygdala is present in a diverse range of vertebrate species, such as lizards, rodents, and primates; however, its structure and connectivity differs across species. The increased connections to visual sensory areas in primate species suggests that understanding the visual selectivity of the amygdala in detail is critical to revealing the principles underlying its function in primate cognition. Therefore, we designed a high-resolution, contrast-agent enhanced, event-related fMRI experiment, and scanned 3 adult rhesus macaques, while they viewed 96 naturalistic stimuli. Half of these stimuli were social (defined by the presence of a conspecific), the other half were nonsocial. We also nested manipulations of emotional valence (positive, neutral, and negative) and visual category (faces, nonfaces, animate, and inanimate) within the stimulus set. The results reveal widespread effects of emotional valence, with the amygdala responding more on average to inanimate objects and animals than faces, bodies, or social agents in this experimental context. These findings suggest that the amygdala makes a contribution to primate vision that goes beyond an auxiliary role in face or social perception. Furthermore, the results highlight the importance of stimulus selection and experimental design when probing the function of the amygdala and other visually responsive brain regions.

Illusory faces are more likely to be perceived as male than female.

Despite our fluency in reading human faces, sometimes we mistakenly perceive illusory faces in objects, a phenomenon known as face pareidolia. Although illusory faces share some neural mechanisms with real faces, it is unknown to what degree pareidolia engages higher-level social perception beyond the detection of a face. In a series of large-scale behavioral experiments (ntotal = 3,815 adults), we found that illusory faces in inanimate objects are readily perceived to have a specific emotional expression, age, and gender. Most strikingly, we observed a strong bias to perceive illusory faces as male rather than female. This male bias could not be explained by preexisting semantic or visual gender associations with the objects, or by visual features in the images. Rather, this robust bias in the perception of gender for illusory faces reveals a cognitive bias arising from a broadly tuned face evaluation system in which minimally viable face percepts are more likely to be perceived as male.

Real Face Value: The Processing of Naturalistic Facial Expressions in the Macaque Inferior Temporal Cortex.

For primates, expressions of fear are thought to be powerful social signals. In laboratory settings, faces with fearful expressions have reliably evoked valence effects in inferior temporal cortex. However, because macaques use so called "fear grins" in a variety of different contexts, the deeper question is whether the macaque inferior temporal cortex is tuned to the prototypical fear grin, or to conspecifics signaling fear? In this study, we combined neuroimaging with the results of a behavioral task to investigate how macaques encode a wide variety of fearful facial expressions. In Experiment 1, we identified two sets of macaque face stimuli using different approaches; we selected faces based on the emotional context (i.e., calm vs. fearful), and we selected faces based on the engagement of action units (i.e., neutral vs. fear grins). We also included human faces in Experiment 1. Then, using fMRI, we found that the faces selected based on context elicited a larger valence effect in the inferior temporal cortex than faces selected based on visual appearance. Furthermore, human facial expressions only elicited weak valence effects. These observations were further supported by the results of a two-alternative, forced-choice task (Experiment 2), suggesting that fear grins vary in their perceived pleasantness. Collectively, these findings indicate that the macaque inferior temporal cortex is more involved in social intelligence than commonly assumed, encoding emergent properties in naturalistic face stimuli that transcend basic visual features. These results demand a rethinking of theories surrounding the function and operationalization of primate inferior temporal cortex.

Clutter substantially reduces selectivity for peripheral faces in the macaque brain.

According to a prominent view in neuroscience, visual stimuli are coded by discrete cortical networks that respond preferentially to specific categories, such as faces or objects. However, it remains unclear how these category-selective networks respond when viewing conditions are cluttered, i.e., when there is more than one stimulus in the visual field. Here, we asked three questions: (1) Does clutter reduce the response and selectivity for faces as a function of retinal location? (2) Is the preferential response to faces uniform across the visual field? And (3) Does the ventral visual pathway encode information about the location of cluttered faces? We used fMRI to measure the response of the face-selective network in awake, fixating macaques (2 female, 5 male). Across a series of four experiments, we manipulated the presence and absence of clutter, as well as the location of the faces relative to the fovea. We found that clutter reduces the response to peripheral faces. When presented in isolation, without clutter, the selectivity for faces is fairly uniform across the visual field, but, when clutter is present, there is a marked decrease in the selectivity for peripheral faces. We also found no evidence of a contralateral visual field bias when faces were presented in clutter. Nonetheless, multivariate analyses revealed that the location of cluttered faces could be decoded from the multivoxel response of the face-selective network. Collectively, these findings demonstrate that clutter blunts the selectivity of the face-selective network to peripheral faces, although information about their retinal location is retained.SIGNIFICANCE STATEMENTNumerous studies that have measured brain activity in macaques have found visual regions that respond preferentially to faces. Although these regions are thought to be essential for social behavior, their responses have typically been measured while faces were presented in isolation, a situation atypical of the real world. How do these regions respond when faces are presented with other stimuli? We report that, when clutter is present, the preferential response to foveated faces is spared but preferential response to peripheral faces is reduced. Our results indicate that the presence of clutter changes the response of the face-selective network.

Preliminary evidence of an increased susceptibility to face pareidolia in postpartum women.

As primates, we are hypersensitive to faces and face-like patterns in the visual environment, hence we often perceive illusory faces in otherwise inanimate objects, such as burnt pieces of toast and the surface of the moon. Although this phenomenon, known as face pareidolia, is a common experience, it is unknown whether our susceptibility to face pareidolia is static across our lifespan or what factors would cause it to change. Given the evidence that behaviour towards face stimuli is modulated by the neuropeptide oxytocin (OT), we reasoned that participants in stages of life associated with high levels of endogenous OT might be more susceptible to face pareidolia than participants in other stages of life. We tested this hypothesis by assessing pareidolia susceptibility in two groups of women; pregnant women (low endogenous OT) and postpartum women (high endogenous OT). We found evidence that postpartum women report seeing face pareidolia more easily than women who are currently pregnant. These data, collected online, suggest that our sensitivity to face-like patterns is not fixed and may change throughout adulthood, providing a crucial proof of concept that requires further research.

Predictive extrapolation effects can have a greater impact on visual decisions, while visual adaptation has a greater impact on conscious visual experience.

Human vision is shaped by historic and by predictive processes. The lingering impact of visual adaptation, for instance, can act to exaggerate differences between past and present inputs, whereas predictive processes can promote extrapolation effects that allow us to anticipate the near future. It is unclear to what extent either of these effects manifest in changes to conscious visual experience. It is also unclear how these influences combine, when acting in concert or opposition. We had people make decisions about the sizes of inputs, and report on levels of decisional confidence. Tests were either selectively subject to size adaptation, to an extrapolation effect, or to both of these effects. When these two effects were placed in opposition, extrapolation had a greater impact on decision making. However, our data suggest the influence of extrapolation is primarily decisional, whereas size adaptation more fully manifests in changes to conscious visual awareness.

Single-Unit Recordings Reveal the Selectivity of a Human Face Area.

The exquisite capacity of primates to detect and recognize faces is crucial for social interactions. Although disentangling the neural basis of human face recognition remains a key goal in neuroscience, direct evidence at the single-neuron level is limited. We recorded from face-selective neurons in human visual cortex in a region characterized by functional magnetic resonance imaging (fMRI) activations for faces compared with objects. The majority of visually responsive neurons in this fMRI activation showed strong selectivity at short latencies for faces compared with objects. Feature-scrambled faces and face-like objects could also drive these neurons, suggesting that this region is not tightly tuned to the visual attributes that typically define whole human faces. These single-cell recordings within the human face processing system provide vital experimental evidence linking previous imaging studies in humans and invasive studies in animal models.SIGNIFICANCE STATEMENT We present the first recordings of face-selective neurons in or near an fMRI-defined patch in human visual cortex. Our unbiased multielectrode array recordings (i.e., no selection of neurons based on a search strategy) confirmed the validity of the BOLD contrast (faces-objects) in humans, a finding with implications for all human imaging studies. By presenting faces, feature-scrambled faces, and face-pareidolia (perceiving faces in inanimate objects) stimuli, we demonstrate that neurons at this level of the visual hierarchy are broadly tuned to the features of a face, independent of spatial configuration and low-level visual attributes.

Parallel Processing of Facial Expression and Head Orientation in the Macaque Brain.

When we move the features of our face, or turn our head, we communicate changes in our internal state to the people around us. How this information is encoded and used by an observer's brain is poorly understood. We investigated this issue using a functional MRI adaptation paradigm in awake male macaques. Among face-selective patches of the superior temporal sulcus (STS), we found a double dissociation of areas processing facial expression and those processing head orientation. The face-selective patches in the STS fundus were most sensitive to facial expression, as was the amygdala, whereas those on the lower, lateral edge of the sulcus were most sensitive to head orientation. The results of this study reveal a new dimension of functional organization, with face-selective patches segregating within the STS. The findings thus force a rethinking of the role of the face-processing system in representing subject-directed actions and supporting social cognition.SIGNIFICANCE STATEMENT When we are interacting with another person, we make inferences about their emotional state based on visual signals. For example, when a person's facial expression changes, we are given information about their feelings. While primates are thought to have specialized cortical mechanisms for analyzing the identity of faces, less is known about how these mechanisms unpack transient signals, like expression, that can change from one moment to the next. Here, using an fMRI adaptation paradigm, we demonstrate that while the identity of a face is held constant, there are separate mechanisms in the macaque brain for processing transient changes in the face's expression and orientation. These findings shed new light on the function of the face-processing system during social exchanges.

A shared mechanism for facial expression in human faces and face pareidolia.

Facial expressions are vital for social communication, yet the underlying mechanisms are still being discovered. Illusory faces perceived in objects (face pareidolia) are errors of face detection that share some neural mechanisms with human face processing. However, it is unknown whether expression in illusory faces engages the same mechanisms as human faces. Here, using a serial dependence paradigm, we investigated whether illusory and human faces share a common expression mechanism. First, we found that images of face pareidolia are reliably rated for expression, within and between observers, despite varying greatly in visual features. Second, they exhibit positive serial dependence for perceived facial expression, meaning an illusory face (happy or angry) is perceived as more similar in expression to the preceding one, just as seen for human faces. This suggests illusory and human faces engage similar mechanisms of temporal continuity. Third, we found robust cross-domain serial dependence of perceived expression between illusory and human faces when they were interleaved, with serial effects larger when illusory faces preceded human faces than the reverse. Together, the results support a shared mechanism for facial expression between human faces and illusory faces and suggest that expression processing is not tightly bound to human facial features.

Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys.

In free-viewing experiments, primates orient preferentially toward faces and face-like stimuli. To investigate the neural basis of this behavior, we measured the spontaneous viewing preferences of monkeys with selective bilateral amygdala lesions. The results revealed that when faces and nonface objects were presented simultaneously, monkeys with amygdala lesions had no viewing preference for either conspecific faces or illusory facial features in everyday objects. Instead of directing eye movements toward socially relevant features in natural images, we found that, after amygdala loss, monkeys are biased toward features with increased low-level salience. We conclude that the amygdala has a role in our earliest specialized response to faces, a behavior thought to be a precursor for efficient social communication and essential for the development of face-selective cortex.

Robust representations of individual faces in chimpanzees (Pan troglodytes) but not monkeys (Macaca mulatta).

Being able to recognize the faces of our friends and family members no matter where we see them represents a substantial challenge for the visual system because the retinal image of a face can be degraded by both changes in the person (age, expression, pose, hairstyle, etc.) and changes in the viewing conditions (direction and degree of illumination). Yet most of us are able to recognize familiar people effortlessly. A popular theory for how face recognition is achieved has argued that the brain stabilizes facial appearance by building average representations that enhance diagnostic features that reliably vary between people while diluting features that vary between instances of the same person. This explains why people find it easier to recognize average images of people, created by averaging multiple images of the same person together, than single instances (i.e. photographs). Although this theory is gathering momentum in the psychological and computer sciences, there is no evidence of whether this mechanism represents a unique specialization for individual recognition in humans. Here we tested two species, chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta), to determine whether average images of different familiar individuals were easier to discriminate than photographs of familiar individuals. Using a two-alternative forced-choice, match-to-sample procedure, we report a behaviour response profile that suggests chimpanzees encode the faces of conspecifics differently than rhesus monkeys and in a manner similar to humans.

Neural Correlate of the Thatcher Face Illusion in a Monkey Face-Selective Patch.

Compelling evidence that our sensitivity to facial structure is conserved across the primate order comes from studies of the "Thatcher face illusion": humans and monkeys notice changes in the orientation of facial features (e.g., the eyes) only when faces are upright, not when faces are upside down. Although it is presumed that face perception in primates depends on face-selective neurons in the inferior temporal (IT) cortex, it is not known whether these neurons respond differentially to upright faces with inverted features. Using microelectrodes guided by functional MRI mapping, we recorded cell responses in three regions of monkey IT cortex. We report an interaction in the middle lateral face patch (ML) between the global orientation of a face and the local orientation of its eyes, a response profile consistent with the perception of the Thatcher illusion. This increased sensitivity to eye orientation in upright faces resisted changes in screen location and was not found among face-selective neurons in other areas of IT cortex, including neurons in another face-selective region, the anterior lateral face patch. We conclude that the Thatcher face illusion is correlated with a pattern of activity in the ML that encodes faces according to a flexible holistic template.

Faces in Context: Does Face Perception Depend on the Orientation of the Visual Scene?

The mechanisms held responsible for familiar face recognition are thought to be orientation dependent; inverted faces are more difficult to recognize than their upright counterparts. Although this effect of inversion has been investigated extensively, researchers have typically sliced faces from photographs and presented them in isolation. As such, it is not known whether the perceived orientation of a face is inherited from the visual scene in which it appears. Here, we address this question by measuring performance in a simultaneous same-different task while manipulating both the orientation of the faces and the scene. We found that the face inversion effect survived scene inversion. Nonetheless, an improvement in performance when the scene was upside down suggests that sensitivity to identity increased when the faces were more easily segmented from the scene. Thus, while these data identify congruency with the visual environment as a contributing factor in recognition performance, they imply different mechanisms operate on upright and inverted faces.

The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions.

It is widely believed that face processing in the primate brain occurs in a network of category-selective cortical regions. Combined functional MRI (fMRI)-single-cell recording studies in macaques have identified high concentrations of neurons that respond more to faces than objects within face-selective patches. However, cells with a preference for faces over objects are also found scattered throughout inferior temporal (IT) cortex, raising the question whether face-selective cells inside and outside of the face patches differ functionally. Here, we compare the properties of face-selective cells inside and outside of face-selective patches in the IT cortex by means of an image manipulation that reliably disrupts behavior toward face processing: inversion. We recorded IT neurons from two fMRI-defined face-patches (ML and AL) and a region outside of the face patches (herein labeled OUT) during upright and inverted face stimulation. Overall, turning faces upside down reduced the firing rate of face-selective cells. However, there were differences among the recording regions. First, the reduced neuronal response for inverted faces was independent of stimulus position, relative to fixation, in the face-selective patches (ML and AL) only. Additionally, the effect of inversion for face-selective cells in ML, but not those in AL or OUT, was impervious to whether the neurons were initially searched for using upright or inverted stimuli. Collectively, these results show that face-selective cells differ in their functional characteristics depending on their anatomicofunctional location, suggesting that upright faces are preferably coded by face-selective cells inside but not outside of the fMRI-defined face-selective regions of the posterior IT cortex.

The face pareidolia illusion drives a happy face advantage that is dependent on perceived gender.

The happy face advantage, the faster recognition of happy than of negative, angry or fearful, emotional expressions, has been reliably found and is modulated by social category cues, such as perceived gender, that is, is larger on female than on male faces. In this study, we tested whether this pattern of results is unique to human faces by investigating whether ambient examples of face pareidolia can also evoke a happy face advantage that is dependent on perceived gender. "Face pareidolia" describes the illusion of facial structure on inanimate objects, such as a tree trunk or a piece of burnt toast. While it has been shown that these illusory faces have expressions that can be recognized by participants, it is unknown whether they drive the same behavioral biases as real facial expressions. Thus, we measured the speed and accuracy with which the expressions of illusory faces that are perceived as female or male are recognized as happy or angry. We found a robust happy face advantage for illusory faces that were rated as more feminine in appearance. Concomitantly, we also found a robust angry face advantage for illusory faces that were rated as more masculine in appearance. Taken together, these findings demonstrate that illusory faces confer the same behavioral advantages as human faces. They also suggest that both perceived emotion and perceived gender are powerful socioevaluative dimensions that are extracted from visual stimuli that merely resemble human faces. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Oxytocin differentially modulates the early neural responses to faces and non-social stimuli.

Oxytocin (OT) alters social cognition partly through effects on the processing and appraisal of faces. It is debated whether the hormone also impacts the processing of other, non-social, visual stimuli. To this end, we conducted a randomized, counter-balanced, double-blind, placebo (PL)-controlled within-subjects' electro-encephalography (EEG) study with cismale participants (to control for gender dimorphic hormonal effects; n = 37). Participants received intranasal OT (24IU) and completed a one-back task viewing emotional (fearful/ happy) and neutral faces, and threat (snakes/spiders) and non-threat (mushrooms/flowers) non-social stimuli. OT differentially impacted event-related potentials (ERP)s to faces and non-social stimuli. For faces regardless of emotion, OT evoked greater occipital N1 and anterior P1 amplitudes at ∼155 ms than after PL, and lead to sustained differences over anterior, bilateral parietal and occipital sites from 205 ms onwards. For all non-social stimuli, OT evoked greater right parietal N1 amplitudes, and later only impacted threat stimuli over right parietal and occipital sites. None of these OT-induced modulations was related to individual anxiety levels. This pattern of results indicates that OT differentially modulates the processing of faces and non-social stimuli, and that the hormone's effect on visual processing and cognition does not occur as a function of non-clinical levels of anxiety.

A behavioral advantage for the face pareidolia illusion in peripheral vision.

Investigation of visual illusions helps us understand how we process visual information. For example, face pareidolia, the misperception of illusory faces in objects, could be used to understand how we process real faces. However, it remains unclear whether this illusion emerges from errors in face detection or from slower, cognitive processes. Here, our logic is straightforward; if examples of face pareidolia activate the mechanisms that rapidly detect faces in visual environments, then participants will look at objects more quickly when the objects also contain illusory faces. To test this hypothesis, we sampled continuous eye movements during a fast saccadic choice task-participants were required to select either faces or food items. During this task, pairs of stimuli were positioned close to the initial fixation point or further away, in the periphery. As expected, the participants were faster to look at face targets than food targets. Importantly, we also discovered an advantage for food items with illusory faces but, this advantage was limited to the peripheral condition. These findings are among the first to demonstrate that the face pareidolia illusion persists in the periphery and, thus, it is likely to be a consequence of erroneous face detection.

How the Thatcher illusion reveals evolutionary differences in the face processing of primates.

Face recognition in humans is a complex cognitive skill that requires sensitivity to unique configurations of eyes, mouth, and other facial features. The Thatcher illusion has been used to demonstrate the importance of orientation when processing configural information within faces. Transforming an upright face so that the eyes and mouth are inverted renders the face grotesque; however, when this "Thatcherized" face is inverted, the effect disappears. Due to the use of primate models in social cognition research, it is important to determine the extent to which specialized cognitive functions like face processing occur across species. To date, the Thatcher illusion has been explored in only a few species with mixed results. Here, we used computerized tasks to examine whether nonhuman primates perceive the Thatcher illusion. Chimpanzees and rhesus monkeys were required to discriminate between Thatcherized and unaltered faces presented upright and inverted. Our results confirm that chimpanzees perceived the Thatcher illusion, but rhesus monkeys did not, suggesting species differences in the importance of configural information in face processing. Three further experiments were conducted to understand why our results differed from previously published accounts of the Thatcher illusion in rhesus monkeys.

Assessing the perception of face pareidolia in children (Homo sapiens), rhesus monkeys (Macaca mulatta), and capuchin monkeys (Sapajus apella).

Face pareidolia is the misperception of a face in an inanimate object and is a common feature of the face detection system in humans. Whereas there are many similarities in how humans and nonhuman animals such as monkeys perceive and respond to faces, it is still unclear whether other species also perceive certain nonface stimuli as faces. We presented a novel computerized task to capuchin monkeys (Sapajus apella), rhesus monkeys (Macaca mulatta), and preschool-aged children (Homo sapiens). This task trained subjects to choose faces over nonface images, and then presented pareidolia images with nonface images. All species selected faces most often on trials that included face images. However, only children selected pareidolia images at levels above chance. These results indicate that while children report perceiving face pareidolia, monkeys do not. These species differences could be due to human-unique experiences that result in an increased aptitude for anthropomorphizing objects with face-like patterns. It could also be due to monkeys showing a greater reliance on stimulus features rather than global, holistically organized cues that faces provide. (PsycInfo Database Record (c) 2023 APA, all rights reserved).