Neuropsychological and neuroanatomical underpinnings of the face pareidolia errors on the noise pareidolia test in patients with mild cognitive impairment and dementia due to Lewy bodies.

OBJECTIVE: Prior research on the Noise Pareidolia Test (NPT) has demonstrated its clinical utility in detecting patients with mild cognitive impairment and dementia due to Lewy Body Disease (LBD). However, few studies to date have investigated the neuropsychological factors underlying pareidolia errors on the NPT across the clinical spectrum of LBD. Furthermore, to our knowledge, no research has examined the relationship between cortical thickness using MRI data and NPT subscores. As such, this study sought to explore the neuropsychological and neuroanatomical factors influencing performance on the NPT utilizing the National Alzheimer's Coordinating Center Lewy Body Dementia Module. METHODS: Our sample included participants with normal cognition (NC; n = 56), LBD with mild cognitive impairment (LBD-MCI; n = 97), and LBD with dementia (LBD-Dementia; n = 94). Archival data from NACC were retrospectively analyzed for group differences in neuropsychological test scores and cognitive and psychiatric predictors of NPT scores. Clinicoradiological correlates between NPT subscores and a small subsample of the above LBD participants were also examined. RESULTS: Analyses revealed significant differences in NPT scores among groups. Regression analysis demonstrated that dementia severity, attention, and visuospatial processing contributed approximately 24% of NPT performance in LBD groups. Clinicoradiological analysis suggests a potential contribution of the right fusiform gyrus, but not the inferior occipital gyrus, to NPT pareidolia error scores. CONCLUSIONS: Our findings highlight the interplay of attention and visuoperceptual functions in complex pareidolia in LBD. Further investigation is needed to refine the utility of NPT scores in clinical settings, including identifying patients at risk for visual illusions and hallucinations.

Dynamic brain communication underwriting face pareidolia.

Face pareidolia is a tendency to seeing faces in nonface images that reflects high tuning to a face scheme. Yet, studies of the brain networks underwriting face pareidolia are scarce. Here, we examined the time course and dynamic topography of gamma oscillatory neuromagnetic activity while administering a task with nonface images resembling a face. Images were presented either with canonical orientation or with display inversion that heavily impedes face pareidolia. At early processing stages, the peaks in gamma activity (40 to 45 Hz) to images either triggering or not face pareidolia originate mainly from the right medioventral and lateral occipital cortices, rostral and caudal cuneus gyri, and medial superior occipital gyrus. Yet, the difference occurred at later processing stages in the high-frequency range of 80 to 85 Hz over a set of the areas constituting the social brain. The findings speak rather for a relatively late neural network playing a key role in face pareidolia. Strikingly, a cutting-edge analysis of brain connectivity unfolding over time reveals mutual feedforward and feedback intra- and interhemispheric communication not only within the social brain but also within the extended large-scale network of down- and upstream regions. In particular, the superior temporal sulcus and insula strongly engage in communication with other brain regions either as signal transmitters or recipients throughout the whole processing of face-pareidolia images.

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.

Children perceive illusory faces in objects as male more often than female.

Face pareidolia is the experience of seeing illusory faces in inanimate objects. While children experience face pareidolia, it is unknown whether they perceive gender in illusory faces, as their face evaluation system is still developing in the first decade of life. In a sample of 412 children and adults from 4 to 80 years of age we found that like adults, children perceived many illusory faces in objects to have a gender and had a strong bias to see them as male rather than female, regardless of their own gender identification. These results provide evidence that the male bias for face pareidolia emerges early in life, even before the ability to discriminate gender from facial cues alone is fully developed. Further, the existence of a male bias in children suggests that any social context that elicits the cognitive bias to see faces as male has remained relatively consistent across generations.

The cortical and subcortical correlates of face pareidolia in the macaque brain.

Face detection is a foundational social skill for primates. This vital function is thought to be supported by specialized neural mechanisms; however, although several face-selective regions have been identified in both humans and nonhuman primates, there is no consensus about which region(s) are involved in face detection. Here, we used naturally occurring errors of face detection (i.e. objects with illusory facial features referred to as examples of 'face pareidolia') to identify regions of the macaque brain implicated in face detection. Using whole-brain functional magnetic resonance imaging to test awake rhesus macaques, we discovered that a subset of face-selective patches in the inferior temporal cortex, on the lower lateral edge of the superior temporal sulcus, and the amygdala respond more to objects with illusory facial features than matched non-face objects. Multivariate analyses of the data revealed differences in the representation of illusory faces across the functionally defined regions of interest. These differences suggest that the cortical and subcortical face-selective regions contribute uniquely to the detection of facial features. We conclude that face detection is supported by a multiplexed system in the primate brain.

Staring death in the face: chimpanzees' attention towards conspecific skulls and the implications of a face module guiding their behaviour.

Chimpanzees exhibit a variety of behaviours surrounding their dead, although much less is known about how they respond towards conspecific skeletons. We tested chimpanzees' visual attention to images of conspecific and non-conspecific stimuli (cat/chimp/dog/rat), shown simultaneously in four corners of a screen in distinct orientations (frontal/diagonal/lateral) of either one of three types (faces/skulls/skull-shaped stones). Additionally, we compared their visual attention towards chimpanzee-only stimuli (faces/skulls/skull-shaped stones). Lastly, we tested their attention towards specific regions of chimpanzee skulls. We theorized that chimpanzee skulls retaining face-like features would be perceived similarly to chimpanzee faces and thus be subjected to similar biases. Overall, supporting our hypotheses, the chimpanzees preferred conspecific-related stimuli. The results showed that chimpanzees attended: (i) significantly longer towards conspecific skulls than other species skulls (particularly in forward-facing and to a lesser extent diagonal orientations); (ii) significantly longer towards conspecific faces than other species faces at forward-facing and diagonal orientations; (iii) longer towards chimpanzee faces compared with chimpanzee skulls and skull-shaped stones, and (iv) attended significantly longer to the teeth, similar to findings for elephants. We suggest that chimpanzee skulls retain relevant, face-like features that arguably activate a domain-specific face module in chimpanzees' brains, guiding their attention.

Rapid neural categorization of facelike objects predicts the perceptual awareness of a face (face pareidolia).

The human brain rapidly and automatically categorizes faces vs. other visual objects. However, whether face-selective neural activity predicts the subjective experience of a face - perceptual awareness - is debated. To clarify this issue, here we use face pareidolia, i.e., the illusory perception of a face, as a proxy to relate the neural categorization of a variety of facelike objects to conscious face perception. In Experiment 1, scalp electroencephalogram (EEG) is recorded while pictures of human faces or facelike objects - in different stimulation sequences - are interleaved every second (i.e., at 1 Hz) in a rapid 6-Hz train of natural images of nonface objects. Participants do not perform any explicit face categorization task during stimulation, and report whether they perceived illusory faces post-stimulation. A robust categorization response to facelike objects is identified at 1 Hz and harmonics in the EEG frequency spectrum with a facelike occipito-temporal topography. Across all individuals, the facelike categorization response is of about 20% of the response to human faces, but more strongly right-lateralized. Critically, its amplitude is much larger in participants who report having perceived illusory faces. In Experiment 2, facelike or matched nonface objects from the same categories appear at 1 Hz in sequences of nonface objects presented at variable stimulation rates (60 Hz to 12 Hz) and participants explicitly report after each sequence whether they perceived illusory faces. The facelike categorization response already emerges at the shortest stimulus duration (i.e., 17 ms at 60 Hz) and predicts the behavioral report of conscious perception. Strikingly, neural facelike-selectivity emerges exclusively when participants report illusory faces. Collectively, these experiments characterize a neural signature of face pareidolia in the context of rapid categorization, supporting the view that face-selective brain activity reliably predicts the subjective experience of a face from a single glance at a variety of stimuli.

The involvement of monocular channels in the face pareidolia effect.

Studies examining the neural mechanisms of face perception in humans have mainly focused on cortical networks of face-selective regions. However, subcortical regions are known to play a significant role in face perception as well. For instance, upon presenting pairs of faces sequentially to the same eye or to different eyes, superior performance is observed in the former condition. This superiority was explained by monocular, pre-striate processing of face stimuli. One of the intriguing face-related effects is the face pareidolia phenomenon, wherein observers perceive faces in inanimate objects. In this study, we examined whether face pareidolia involves similar low-level neural substrates to those that are involved in face perception. We presented participants with pairs of houses or face-like houses using a stereoscope to manipulate the information presented to each eye and asked them to determine whether the stimuli were similar or different. We managed to examine the contribution of monocular channels (mostly subcortical) in processing face-like stimuli. We hypothesized that besides their involvement in actual face perception, subcortical structures are engaged in face pareidolia as well. To test our hypothesis, we conducted three experiments to replicate and strengthen the reliability of our results and rule out alternative explanations. We demonstrated a perceptual benefit when presenting similar face-like houses to the same eye in comparison to their presentation to different eyes. This finding matches previous results found for images of real faces and indicates subcortical involvement not only in face perception but also in processing face-like objects.

Odor-driven face-like categorization in the human infant brain.

Understanding how the young infant brain starts to categorize the flurry of ambiguous sensory inputs coming in from its complex environment is of primary scientific interest. Here, we test the hypothesis that senses other than vision play a key role in initiating complex visual categorizations in 20 4-mo-old infants exposed either to a baseline odor or to their mother's odor while their electroencephalogram (EEG) is recorded. Various natural images of objects are presented at a 6-Hz rate (six images/second), with face-like object configurations of the same object categories (i.e., eliciting face pareidolia in adults) interleaved every sixth stimulus (i.e., 1 Hz). In the baseline odor context, a weak neural categorization response to face-like stimuli appears at 1 Hz in the EEG frequency spectrum over bilateral occipitotemporal regions. Critically, this face-like-selective response is magnified and becomes right lateralized in the presence of maternal body odor. This reveals that nonvisual cues systematically associated with human faces in the infant's experience shape the interpretation of face-like configurations as faces in the right hemisphere, dominant for face categorization. At the individual level, this intersensory influence is particularly effective when there is no trace of face-like categorization in the baseline odor context. These observations provide evidence for the early tuning of face-(like)-selective activity from multisensory inputs in the developing brain, suggesting that perceptual development integrates information across the senses for efficient category acquisition, with early maturing systems such as olfaction driving the acquisition of categories in later-developing systems such as vision.

Face Tuning in Depression.

The latest COVID-19 pandemic reveals that unexpected changes elevate depression bringing people apart, but also calling for social sharing. Yet the impact of depression on social cognition and functioning is not well understood. Assessment of social cognition is crucial not only for a better understanding of major depressive disorder (MDD), but also for screening, intervention, and remediation. Here by applying a novel experimental tool, a Face-n-Food task comprising a set of images bordering on the Giuseppe Arcimboldo style, we assessed the face tuning in patients with MDD and person-by-person matched controls. The key benefit of these images is that single components do not trigger face processing. Contrary to common beliefs, the outcome indicates that individuals with depression express intact face responsiveness. Yet, while in depression face sensitivity is tied with perceptual organization, in typical development, it is knotted with social cognition capabilities. Face tuning in depression, therefore, may rely upon altered behavioral strategies and underwriting brain mechanisms. To exclude a possible camouflaging effect of female social skills, we examined gender impact. Neither in depression nor in typical individuals had females excelled in face tuning. The outcome sheds light on the origins of the face sensitivity and alterations in social functioning in depression and mental well-being at large. Aberrant social functioning in depression is likely to be the result of deeply-rooted maladaptive strategies rather than of poor sensitivity to social signals. This has implications for mental well-being under the current pandemic conditions.

What does a "face cell" want?'

In the 1970s Charlie Gross was among the first to identify neurons that respond selectively to faces, in the macaque inferior temporal (IT) cortex. This seminal finding has been followed by numerous studies quantifying the visual features that trigger a response from face cells in order to answer the question; what do face cells want? However, the connection between face-selective activity in IT cortex and visual perception remains only partially understood. Here we present fMRI results in the macaque showing that some face patches respond to illusory facial features in objects. We argue that to fully understand the functional role of face cells, we need to develop approaches that test the extent to which their response explains what we see.

Face pareidolia in schizophrenia.

BACKGROUND: Faces convey valuable daily life social signals. As in most psychiatric conditions, non-verbal social cognition or its components including face processing may be aberrant in schizophrenia (SZ). Social participation of individuals with SZ is vital for their quality of life, and remediation of social abilities in this population is of high relevance both for society and clinical care. METHOD: Tuning to faces in non-face images such as shadows, grilled toasts, or ink blots is called face pareidolia. Humans possess high sensitivity to facial signals: even fetuses and infants are well tuned to coarse face cues. Here we assessed face tuning in individuals with SZ and person-by-person matched controls by using a new experimental tool, a set of food-plate images bordering on the Giuseppe Arcimboldo style. The key benefit of these images is that single components do not trigger face processing. RESULTS AND CONCLUSIONS: The outcome indicates that individuals with SZ exhibit aberrant face tuning in face-like non-face images (χ2(1) = 17.44, p = 0.0001) that can hamper adaptive interaction with peers and social participation hindering, in turn, clinical remediation. Face response rate in SZ patients was related to the scores on the event arrangement task tapping social cognition (Pearson product-moment correlation, r = 0.602, p = 0.01) and on picture completion task assessing visual perceptual organization (Spearman's rho = 0.614, p = 0.009). Therefore, poor performance on the face tuning task is unlikely to be accounted for by deviant general cognitive abilities, but rather by impairments in perceptual integration and social cognition. Comparison of these findings with data in autism and other neuropsychiatric conditions provides novel insights on the origins of face tuning in SZ and triggers brain imaging research.

Changes in face and face pareidolia processing in patients with migraine: an ERP study.

Migraine is a multifactorial brain disorder characterized by recurrent disabling headache attacks. One of the possible mechanisms in the pathogenesis of migraine may be a decrease in inhibitory cortical stimuli in the primary visual cortex attributable to cortical hyperexcitability. The aim of this study was to investigate the neural correlates underlying face and face pareidolia processing in terms of the event-related potential (ERP) components, N170, vertex positive potential (VPP), and N250, in patients with migraine. In total, 40 patients with migraine without aura, 23 patients with migraine and aura, and 30 healthy controls were enrolled. We recorded ERPs during the presentation of face and face pareidolia images. N170, VPP, and N250 mean amplitudes and latencies were examined. N170 was significantly greater in patients with migraine with aura than in healthy controls. VPP amplitude was significantly greater in patients with migraine without aura than in healthy controls. The face stimuli evoked significantly earlier VPP responses to faces (168.7 ms, SE = 1.46) than pareidolias (173.4 ms, SE = 1.41) in patients with migraine with aura. We did not find a significant difference between N250 amplitude for face and face pareidolia processing. A significant difference was observed between the groups for pareidolia in terms of N170 [F(2,86) = 14,75, P < 0.001] and VPP [F(2,86) = 16.43, P < 0.001] amplitudes. Early ERPs are a valuable tool to study the neural processing of face processing in patients with migraine to demonstrate visual cortical hyperexcitability.NEW & NOTEWORTHY Event-related potentials (ERPs) are important for understanding face and face pareidolia processing in patients with migraine. N170, vertex positive potential (VPP), and N250 ERPs were investigated. N170 was revealed as a potential component of cortical excitability for face and face pareidolia processing in patients with migraine.

A machine learning approach to predict perceptual decisions: an insight into face pareidolia.

The perception of an external stimulus not only depends upon the characteristics of the stimulus but is also influenced by the ongoing brain activity prior to its presentation. In this work, we directly tested whether spontaneous electrical brain activities in prestimulus period could predict perceptual outcome in face pareidolia (visualizing face in noise images) on a trial-by-trial basis. Participants were presented with only noise images but with the prior information that some faces would be hidden in these images, while their electrical brain activities were recorded; participants reported their perceptual decision, face or no-face, on each trial. Using differential hemispheric asymmetry features based on large-scale neural oscillations in a machine learning classifier, we demonstrated that prestimulus brain activities could achieve a classification accuracy, discriminating face from no-face perception, of 75% across trials. The time-frequency features representing hemispheric asymmetry yielded the best classification performance, and prestimulus alpha oscillations were found to be mostly involved in predicting perceptual decision. These findings suggest a mechanism of how prior expectations in the prestimulus period may affect post-stimulus decision making.

Seeing Jesus in toast: neural and behavioral correlates of face pareidolia.

Face pareidolia is the illusory perception of non-existent faces. The present study, for the first time, contrasted behavioral and neural responses of face pareidolia with those of letter pareidolia to explore face-specific behavioral and neural responses during illusory face processing. Participants were shown pure-noise images but were led to believe that 50% of them contained either faces or letters; they reported seeing faces or letters illusorily 34% and 38% of the time, respectively. The right fusiform face area (rFFA) showed a specific response when participants "saw" faces as opposed to letters in the pure-noise images. Behavioral responses during face pareidolia produced a classification image (CI) that resembled a face, whereas those during letter pareidolia produced a CI that was letter-like. Further, the extent to which such behavioral CIs resembled faces was directly related to the level of face-specific activations in the rFFA. This finding suggests that the rFFA plays a specific role not only in processing of real faces but also in illusory face perception, perhaps serving to facilitate the interaction between bottom-up information from the primary visual cortex and top-down signals from the prefrontal cortex (PFC). Whole brain analyses revealed a network specialized in face pareidolia, including both the frontal and occipitotemporal regions. Our findings suggest that human face processing has a strong top-down component whereby sensory input with even the slightest suggestion of a face can result in the interpretation of a face.