The development of upright face perception depends on evolved orientation-specific mechanisms and experience.

Here we examine whether our impressive ability to perceive upright faces arises from evolved orientation-specific mechanisms, our extensive experience with upright faces, or both factors. To do so, we tested Claudio, a man with a congenital joint disorder causing his head to be rotated back so that it is positioned between his shoulder blades. As a result, Claudio has seen more faces reversed in orientation to his own face than matched to it. Controls exhibited large inversion effects on all tasks, but Claudio performed similarly with upright and inverted faces in both detection and identity-matching tasks, indicating these abilities are the product of evolved mechanisms and experience. In contrast, he showed clear upright superiority when detecting "Thatcherized" faces (faces with vertically flipped features), suggesting experience plays a greater role in this judgment. Together, these findings indicate that both evolved orientation-specific mechanisms and experience contribute to our proficiency with upright faces.

Dissociations between face identity and face expression processing in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DPs) experience severe and lifelong deficits recognising faces, but whether their deficits are selective to the processing of face identity or extend to the processing of face expression remains unclear. Clarifying this issue is important for understanding DP impairments and advancing theories of face processing. We compared identity and expression processing in a large sample of DPs (N = 124) using three different matching tasks that each assessed identity and expression processing with identical experimental formats. We ran each task in upright and inverted orientations and we measured inversion effects to assess the integrity of upright-specific face processes. We report three main results. First, DPs showed large deficits at discriminating identity but only subtle deficits at discriminating expression. Second, DPs showed a reduced inversion effect for identity but a normal inversion effect for expression. Third, DPs' performance on the expression tasks were linked to autism traits, but their performance on the identity tasks were not. These results constitute several dissociations between identity and expression processing in DP, and they are consistent with the view that the core impairment in DP is highly selective to identity.

Contralateral Biases in Category-selective Areas Are Stronger in the Left Hemisphere than the Right Hemisphere.

Contralateral bias is a well-known feature of early visual cortex, but how it varies across higher-level, category-selective visual cortex and how much that bias differs between preferred and nonpreferred is unclear. Here, we examined 12 category-selective regions across 4 experiments using peripherally presented faces, bodies, houses, and scenes, to measure the difference in contralateral bias between preferred and nonpreferred stimuli. The results showed a substantial range of contralateral biases across the category-selective regions, similar to prior studies using category-selective stimuli [Silson, E. H., Groen, I. I., & Baker, C. I. Direct comparison of contralateral bias and face/scene selectivity in human occipitotemporal cortex. Brain Structure and Function, 227, 1405-1421, 2022; Gomez, J., Natu, V., Jeska, B., Barnett, M., & Grill-Spector, K. Development differentially sculpts receptive fields across early and high-level human visual cortex. Nature Communications, 9, 788, 2018; Silson, E. H., Groen, I. I. A., Kravitz, D. J., & Baker, C. I. Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex. Journal of Vision, 16, 14, 2016; Kay, K. N., Weiner, K. S., & Grill-Spector, K. Attention reduces spatial uncertainty in human ventral temporal cortex. Current Biology, 25, 595-600, 2015; Silson, E. H., Chan, A. W.-Y., Reynolds, R. C., Kravitz, D. J., & Baker, C. I. A retinotopic basis for the division of high-level scene processing between lateral and ventral human occipitotemporal cortex. Journal of Neuroscience, 35, 11921-11935, 2015]. These contralateral biases were stronger in the left hemisphere regions than right, an asymmetry that was unchanged even when participants performed an attentionally demanding task. Thus, corresponding pairs of category-selective regions (e.g., left fusiform face area [lFFA] and right FFA [rFFA]) do not appear to be mirror images of each other; instead, the right hemisphere regions engage in greater integration of information from the two hemifields. The rFFA and right fusiform body area-both located on the right lateral fusiform gyrus-consistently had the weakest contralateral biases. That this asymmetry was most pronounced in the fusiform gyrus may account for why a unilateral lesion to the rFFA but not the lFFA can produce prosopagnosia. Together, our findings demonstrate that category-selective areas show pronounced differences in the extent of their contralateral biases and that a consistent asymmetry in the strength of the contralateral biases exists between the two hemispheres.

Music perception in acquired prosopagnosia.

BACKGROUND: Acquired prosopagnosia is often associated with other deficits such as dyschromatopsia and topographagnosia, from damage to adjacent perceptual networks. A recent study showed that some subjects with developmental prosopagnosia also have congenital amusia, but problems with music perception have not been described with the acquired variant. OBJECTIVE: Our goal was to determine if music perception was also impaired in subjects with acquired prosopagnosia, and if so, its anatomic correlate. METHOD: We studied eight subjects with acquired prosopagnosia, all of whom had extensive neuropsychological and neuroimaging testing. They performed a battery of tests evaluating pitch and rhythm processing, including the Montréal Battery for the Evaluation of Amusia. RESULTS: At the group level, subjects with anterior temporal lesions were impaired in pitch perception relative to the control group, but not those with occipitotemporal lesions. Three of eight subjects with acquired prosopagnosia had impaired musical pitch perception while rhythm perception was spared. Two of the three also showed reduced musical memory. These three reported alterations in their emotional experience of music: one reported music anhedonia and aversion, while the remaining two had changes consistent with musicophilia. The lesions of these three subjects affected the right or bilateral temporal poles as well as the right amygdala and insula. None of the three prosopagnosic subjects with lesions limited to the inferior occipitotemporal cortex exhibited impaired pitch perception or musical memory, or reported changes in music appreciation. CONCLUSION: Together with the results of our previous studies of voice recognition, these findings indicate an anterior ventral syndrome that can include the amnestic variant of prosopagnosia, phonagnosia, and various alterations in music perception, including acquired amusia, reduced musical memory, and subjective reports of altered emotional experience of music.

Persistent prosopagnosia following COVID-19.

COVID-19 can cause psychological problems including loss of smell and taste, long-lasting memory, speech, and language impairments, and psychosis. Here, we provide the first report of prosopagnosia following symptoms consistent with COVID-19. Annie is a 28-year-old woman who had normal face recognition prior to contracting COVID-19 in March 2020. Two months later, she noticed face recognition difficulties while experiencing symptom relapses and her deficits with faces have persisted. On two tests of familiar face recognition and two tests of unfamiliar face recognition, Annie showed clear impairments. In contrast, she scored normally on tests assessing face detection, face identity perception, object recognition, scene recognition, and non-visual memory. Navigational deficits frequently co-occur with prosopagnosia, and Annie reports that her navigational abilities are substantially worse than before she became ill. Self-report survey data from 54 respondents with long COVID showed that a majority reported reductions in visual recognition and navigation abilities. In summary, Annie's results indicate that COVID-19 can produce severe and selective neuropsychological impairments similar to deficits seen following brain damage, and it appears that high-level visual impairments are not uncommon in people with long COVID.

Face distortions in prosopometamorphopsia provide new insights into the organization of face perception.

Prosopometamorphopsia (PMO) is a striking condition of visual perception in which facial features appear distorted, for example drooping, swelling, or twisting. Although numerous cases have been reported, few of those investigations have carried out formal testing motivated by theories of face perception. However, because PMO involves conscious visual distortions to faces which participants can report, it can be used to probe fundamental questions about face representations. Here we review cases of PMO that address theoretical questions in visual neuroscience including face specificity, inverted face processing, the importance of the vertical midline, dissociable representations for each half of the face, hemispheric specialization, the relationship between face recognition and conscious face perception, and the reference frames that face representations are embedded within. Finally, we list and touch upon eighteen open questions that make clear how much is left to learn about PMO and the potential it has to provide important advances in face perception.

Hominoid-specific sulcal variability is related to face perception ability.

The relationship among brain structure, brain function, and behavior is of major interest in neuroscience, evolutionary biology, and psychology. This relationship is especially intriguing when considering hominoid-specific brain structures because they cannot be studied in widely examined models in neuroscience such as mice, marmosets, and macaques. The fusiform gyrus (FG) is a hominoid-specific structure critical for face processing that is abnormal in individuals with developmental prosopagnosia (DPs)-individuals who have severe deficits recognizing the faces of familiar people in the absence of brain damage. While previous studies have found anatomical and functional differences in the FG between DPs and NTs, no study has examined the shallow tertiary sulcus (mid-fusiform sulcus, MFS) within the FG that is a microanatomical, macroanatomical, and functional landmark in humans, as well as was recently shown to be present in non-human hominoids. Here, we implemented pre-registered analyses of neuroanatomy and face perception in NTs and DPs. Results show that the MFS was shorter in DPs than NTs. Furthermore, individual differences in MFS length in the right, but not left, hemisphere predicted individual differences in face perception. These results support theories linking brain structure and function to perception, as well as indicate that individual differences in MFS length can predict individual differences in face processing. Finally, these findings add to growing evidence supporting a relationship between morphological variability of late developing, tertiary sulci and individual differences in cognition.

Developmental prosopagnosics and super recognizers rely on the same facial features used by individuals with normal face recognition abilities for face identification.

Face recognition depends on the ability of the face processing system to extract facial features that define the identity of a face. In a recent study we discovered that altering a subset of facial features changed the identity of the face, indicating that they are critical for face identification. Changing another set of features did not change the identity of a face, indicating that they are not critical for face identification. In the current study, we assessed whether developmental prosopagnosics (DPs) and super recognizers (SRs) also rely more heavily on these critical features than non-critical features for face identification. To that end, we presented to DPs and SRs faces in which either the critical or the non-critical features were manipulated. In Study 1, we presented SRs with a famous face recognition task. We found that overall SRs recognized famous faces that differ in either critical or non-critical features better than controls. Similar to controls, changes in critical features had a larger effect on SRs' face recognition than changes in non-critical features. In Study 2, we presented an identity matching task to DPs and SRs. Similar to controls, DPs and SRs perceived faces that differed in critical features as more different than faces that differed in non-critical features. Taken together, our results indicate that SRs and DPs use the same critical features for face identification as normal individuals. These findings emphasize the fundamental role of this subset of features for face identification.

Visual input to the left versus right eye yields differences in face preferences in 3-month-old infants.

From birth, infants prefer looking at faces over scrambled faces. This face input is important for the development of face processing: individuals who experienced early visual deprivation due to congenital cataracts have long-lasting face processing deficits. Interestingly, the deficits are eye-specific such that left eye cataracts disrupt the development of face processing, whereas right eye cataracts do not. This raises the question of whether infant face preferences are driven primarily by faces observed through the left eye. To investigate this, we presented 3-month-old infants with intact faces paired with scrambled faces. Infants viewed the moving stimuli binocularly, only with their left eye, or only with their right eye. Infants viewing stimuli binocularly or with only the left eye spent significantly more time looking at intact faces than scrambled faces, but this effect was equivocal in infants viewing stimuli through only their right eye. Infants in the binocular group had the greatest preference for faces, and this preference was greater than the right eye group's preference for faces. The left eye group's preference for faces was not statistically different from the other two groups' preference for faces, but additional analyses revealed a correlation between preference for faces and age for the right eye group only, indicating that preference for faces seen with the right eye increase from 3 to 4 months of age. These results indicate that the left eye plays a special role in face processing at, or before 3 months of age, but a preference for faces through the right eye emerges soon after.

Face-Specific Perceptual Distortions Reveal A View- and Orientation-Independent Face Template.

The spatial coordinate system in which a stimulus representation is embedded is known as its reference frame. Every visual representation has a reference frame [1], and the visual system uses a variety of reference frames to efficiently code visual information [e.g., 1-5]. The representation of faces in early stages of visual processing depends on retino-centered reference frames, but little is known about the reference frames that code the high-level representations used to make judgements about faces. Here, we focus on a rare and striking disorder of face perception-hemi-prosopometamorphopsia (hemi-PMO)-to investigate these reference frames. After a left splenium lesion, Patient A.D. perceives features on the right side of faces as if they had melted. The same features were distorted when faces were presented in either visual field, at different in-depth rotations, and at different picture-plane orientations including upside-down. A.D.'s results indicate faces are aligned to a view- and orientation-independent face template encoded in a face-centered reference frame, that these face-centered representations are present in both the left and right hemisphere, and that the representations of the left and right halves of a face are dissociable.

Eye movements and retinotopic tuning in developmental prosopagnosia.

Despite extensive investigation, the causes and nature of developmental prosopagnosia (DP)-a severe face identification impairment in the absence of acquired brain injury-remain poorly understood. Drawing on previous work showing that individuals identified as being neurotypical (NT) show robust individual differences in where they fixate on faces, and recognize faces best when the faces are presented at this location, we defined and tested four novel hypotheses for how atypical face-looking behavior and/or retinotopic face encoding could impair face recognition in DP: (a) fixating regions of poor information, (b) inconsistent saccadic targeting, (c) weak retinotopic tuning, and (d) fixating locations not matched to the individual's own face tuning. We found no support for the first three hypotheses, with NTs and DPs consistently fixating similar locations and showing similar retinotopic tuning of their face perception performance. However, in testing the fourth hypothesis, we found preliminary evidence for two distinct phenotypes of DP: (a) Subjects characterized by impaired face memory, typical face perception, and a preference to look high on the face, and (b) Subjects characterized by profound impairments to both face memory and perception and a preference to look very low on the face. Further, while all NTs and upper-looking DPs performed best when faces were presented near their preferred fixation location, this was not true for lower-looking DPs. These results suggest that face recognition deficits in a substantial proportion of people with DP may arise not from aberrant face gaze or compromised retinotopic tuning, but from the suboptimal matching of gaze to tuning.

Object recognition in acquired and developmental prosopagnosia.

Whether face and object recognition are dissociated in prosopagnosia continues to be debated: a recent review highlighted deficiencies in prior studies regarding the evidence for such a dissociation. Our goal was to study cohorts with acquired and developmental prosopagnosia with a complementary battery of tests of object recognition that address prior limitations, as well as evaluating for residual effects of object expertise. We studied 15 subjects with acquired and 12 subjects with developmental prosopagnosia on three tests: the Old/New Tests, the Cambridge Bicycle Memory Test, and the Expertise-adjusted Test of Car Recognition. Most subjects with developmental prosopagnosia were normal on the Old/New Tests: for acquired prosopagnosia, subjects with occipitotemporal lesions often showed impairments while those with anterior temporal lesions did not. Ten subjects showed a putative classical dissociation between the Cambridge Face and Bicycle Memory Tests, seven of whom had normal reaction times. Both developmental and acquired groups showed reduced car recognition on the expertise-adjusted test, though residual effects of expertise were still evident. Two subjects with developmental prosopagnosia met criteria for normal object recognition across all tests. We conclude that strong evidence for intact object recognition can be found in a few subjects but the majority show deficits, particularly those with the acquired form. Both acquired and developmental forms show residual but reduced object expertise effects.

Perception of musical pitch in developmental prosopagnosia.

Studies of developmental prosopagnosia have often shown that developmental prosopagnosia differentially affects human face processing over non-face object processing. However, little consideration has been given to whether this condition is associated with perceptual or sensorimotor impairments in other modalities. Comorbidities have played a role in theories of other developmental disorders such as dyslexia, but studies of developmental prosopagnosia have often focused on the nature of the visual recognition impairment despite evidence for widespread neural anomalies that might affect other sensorimotor systems. We studied 12 subjects with developmental prosopagnosia with a battery of auditory tests evaluating pitch and rhythm processing as well as voice perception and recognition. Overall, three subjects were impaired in fine pitch discrimination, a prevalence of 25% that is higher than the estimated 4% prevalence of congenital amusia in the general population. This was a selective deficit, as rhythm perception was unaffected in all 12 subjects. Furthermore, two of the three prosopagnosic subjects who were impaired in pitch discrimination had intact voice perception and recognition, while two of the remaining nine subjects had impaired voice recognition but intact pitch perception. These results indicate that, in some subjects with developmental prosopagnosia, the face recognition deficit is not an isolated impairment but is associated with deficits in other domains, such as auditory perception. These deficits may form part of a broader syndrome which could be due to distributed microstructural anomalies in various brain networks, possibly with a common theme of right hemispheric predominance.

Use of Face Information Varies Systematically From Developmental Prosopagnosics to Super-Recognizers.

Face-recognition abilities differ largely in the neurologically typical population. We examined how the use of information varies with face-recognition ability from developmental prosopagnosics to super-recognizers. Specifically, we investigated the use of facial features at different spatial scales in 112 individuals, including 5 developmental prosopagnosics and 8 super-recognizers, during an online famous-face-identification task using the bubbles method. We discovered that viewing of the eyes and mouth to identify faces at relatively high spatial frequencies is strongly correlated with face-recognition ability, evaluated from two independent measures. We also showed that the abilities of developmental prosopagnosics and super-recognizers are explained by a model that predicts face-recognition ability from the use of information built solely from participants with intermediate face-recognition abilities ( n = 99). This supports the hypothesis that the use of information varies quantitatively from developmental prosopagnosics to super-recognizers as a function of face-recognition ability.

Greater reliance on the eye region predicts better face recognition ability.

Interest in using individual differences in face recognition ability to better understand the perceptual and cognitive mechanisms supporting face processing has grown substantially in recent years. The goal of this study was to determine how varying levels of face recognition ability are linked to changes in visual information extraction strategies in an identity recognition task. To address this question, fifty participants completed six tasks measuring face and object processing abilities. Using the Bubbles method (Gosselin & Schyns, 2001), we also measured each individual's use of visual information in face recognition. At the group level, our results replicate previous findings demonstrating the importance of the eye region for face identification. More importantly, we show that face processing ability is related to a systematic increase in the use of the eye area, especially the left eye from the observer's perspective. Indeed, our results suggest that the use of this region accounts for approximately 20% of the variance in face processing ability. These results support the idea that individual differences in face processing are at least partially related to the perceptual extraction strategy used during face identification.

Face-specific and domain-general visual processing deficits in children with developmental prosopagnosia.

Evidence suggests that face and object recognition depend on distinct neural circuitry within the visual system. Work with adults with developmental prosopagnosia (DP) demonstrates that some individuals have preserved object recognition despite severe face recognition deficits. This face selectivity in adults with DP indicates that face- and object-processing systems can develop independently, but it is unclear at what point in development these mechanisms are separable. Determining when individuals with DP first show dissociations between faces and objects is one means to address this question. In the current study, we investigated face and object processing in six children with DP (5-12-years-old). Each child was assessed with one face perception test, two different face memory tests, and two object memory tests that were matched to the face memory tests in format and difficulty. Scores from the DP children on the matched face and object tasks were compared to within-subject data from age-matched controls. Four of the six DP children, including the 5-year-old, showed evidence of face-specific deficits, while one child appeared to have more general visual-processing deficits. The remaining child had inconsistent results. The presence of face-specific deficits in children with DP suggests that face and object perception depend on dissociable processes in childhood.

Word and text processing in developmental prosopagnosia.

The "many-to-many" hypothesis proposes that visual object processing is supported by distributed circuits that overlap for different object categories. For faces and words the hypothesis posits that both posterior fusiform regions contribute to both face and visual word perception and predicts that unilateral lesions impairing one will affect the other. However, studies testing this hypothesis have produced mixed results. We evaluated visual word processing in subjects with developmental prosopagnosia, a condition linked to right posterior fusiform abnormalities. Ten developmental prosopagnosic subjects performed a word-length effect task and a task evaluating the recognition of word content across variations in text style, and the recognition of style across variations in word content. All subjects had normal word-length effects. One had prolonged sorting time for word recognition in handwritten stimuli. These results suggest that the deficit in developmental prosopagnosia is unlikely to affect visual word processing, contrary to predictions of the many-to-many hypothesis.

Localization and patterns of Cerebral dyschromatopsia: A study of subjects with prospagnosia.

OBJECTIVE: Cerebral dyschromatopsia is sometimes associated with acquired prosopagnosia. Given the variability in structural lesions that cause acquired prosopagnosia, this study aimed to investigate the structural correlates of prosopagnosia-associated dyschromatopsia, and to determine if such colour processing deficits could also accompany developmental prosopagnosia. In addition, we studied whether cerebral dyschromatopsia is typified by a consistent pattern of hue impairments. METHODS: We investigated hue discrimination in a cohort of 12 subjects with acquired prosopagnosia and 9 with developmental prosopagnosia, along with 42 matched controls, using the Farnsworth-Munsell 100-hue test. RESULTS: We found impaired hue discrimination in six subjects with acquired prosopagnosia, five with bilateral and one with a unilateral occipitotemporal lesion. Structural MRI analysis showed maximum overlap of lesions in the right and left lingual and fusiform gyri. Fourier analysis of their error scores showed tritanopic-like deficits and blue-green impairments, similar to tendencies displayed by the healthy controls. Three subjects also showed a novel fourth Fourier component, indicating additional peak deficits in purple and green-yellow regions. No subject with developmental prosopagnosia had impaired hue discrimination. CONCLUSIONS: In our subjects with prosopagnosia, dyschromatopsia occurred in those with acquired lesions of the fusiform gyri, usually bilateral but sometimes unilateral. The dyschromatopsic deficit shows mainly an accentuation of normal tritatanopic-like tendencies. These are sometimes accompanied by additional deficits, although these could represent artifacts of the testing procedure.

Seeing the eyes in acquired prosopagnosia.

Case reports have suggested that perception of the eye region may be impaired more than that of other facial regions in acquired prosopagnosia. However, it is unclear how frequently this occurs, whether such impairments are specific to a certain anatomic subtype of prosopagnosia, and whether these impairments are related to changes in the scanning of faces. We studied a large cohort of 11 subjects with this rare disorder, who had a variety of occipitotemporal or anterior temporal lesions, both unilateral and bilateral. Lesions were characterized by functional and structural imaging. Subjects performed a perceptual discrimination test in which they had to discriminate changes in feature position, shape, or external contour. Test conditions were manipulated to stress focused or divided attention across the whole face. In a second experiment we recorded eye movements while subjects performed a face memory task. We found that greater impairment for eye processing was more typical of subjects with occipitotemporal lesions than those with anterior temporal lesions. This eye selectivity was evident for both eye position and shape, with no evidence of an upper/lower difference for external contour. A greater impairment for eye processing was more apparent under attentionally more demanding conditions. Despite these perceptual deficits, most subjects showed a normal tendency to scan the eyes more than the mouth. We conclude that occipitotemporal lesions are associated with a partially selective processing loss for eye information and that this deficit may be linked to loss of the right fusiform face area, which has been shown to have activity patterns that emphasize the eye region.