Category contingent aftereffects for faces of different races, ages and species

Exposure to faces biases perceptions of subsequently viewed faces such that normality judgments of similar faces are increased. Simultaneously inducing such an aftereffect in opposite directions for two groups of faces might indicate discrete responding of the neural populations coding for those groups. Here we show such "category contingent" aftereffects following exposure to faces differing in eye-spacing (wide versus narrow) for European versus African faces, adult versus infant faces, and human versus monkey faces. As aftereffects reflect changes in responses of neural populations that code faces, our results may then suggest that functionally distinct neural populations code faces of different ages, races and species and that the human brain potentially contains discrete representations of these categories.     

Sex-contingent face aftereffects depend on perceptual category rather than structural encoding

Many studies have used visual adaptation to investigate how recent experience with faces influences perception. While faces similar to those seen during adaptation phases are typically perceived as more 'normal' after adaptation, it is possible to induce aftereffects in one direction for one category (e.g. female) and simultaneously induce aftereffects in the opposite direction for another category (e.g. male). Such aftereffects could reflect 'category-contingent' adaptation of neurons selective for perceptual category (e.g. male or female) or 'structure-contingent' adaptation of lower-level neurons coding the physical characteristics of different face patterns. We compared these explanations by testing for simultaneous opposite after effects following adaptation to (a) two groups of faces from distinct sex categories (male and female) or (b) two groups of faces from the same sex category (female and hyper-female) where the structural differences between the female and hyper-female groups were mathematically identical to those between male and female groups. We were able to induce opposite aftereffects following adaptation between sex categories but not after adaptation within a sex category. These findings indicate the involvement of neurons coding perceptual category in sex-contingent face aftereffects and cannot be explained by neurons coding only the physical aspects of face patterns.     

Effects of normal and abnormal visual experience on the development of opposing aftereffects for upright and inverted faces

We used opposing figural aftereffects to investigate whether there are at least partially separable representations of upright and inverted faces in patients who missed early visual experience because of bilateral congenital cataracts (mean age at test 19.5 years). Visually normal adults and 10-year-olds were tested for comparison. Adults showed the expected opposing aftereffects for upright and inverted faces. Ten-year-olds showed an adultlike aftereffect for upright faces but, unlike the adult group, no aftereffect for inverted faces. Patients failed to show an aftereffect for either upright or inverted faces. Overall, the results suggest that early visual input is necessary for the later development of (at least partially) separable representations of upright and inverted faces, a developmental process that takes many years to reach an adult-like refinement.     

Development of category formation for faces differing by age in 9‐ to 12‐month‐olds: An effect of experience with infant faces

We examined category formation for faces differing in age in 9‐ and 12‐month‐olds, and the influence of exposure to infant faces on such ability. Infants were familiarized with adult or infant faces, and then tested with a novel exemplar from the familiarized category paired with a novel exemplar from a novel category (Experiment 1). Both age groups formed discrete categories of adult and infant faces, but exposure to infant faces in everyday life did not modulate performance. The same task was conducted with child versus infant faces (Experiment 2). Whereas 9‐month‐olds preferred infant faces after familiarization with child faces, but not child faces after familiarization with infant faces, 12‐month‐olds formed discrete categories of child and infant faces. Moreover, more exposure to infant faces correlated with higher novel category preference scores when infants were familiarized with infant faces in 12‐month‐olds, but not 9‐month‐olds. The 9‐month‐old asymmetry did not reflect spontaneous preference for infant over child faces (Experiment 3). These findings indicate that 9‐ and 12‐month‐olds can form age‐based categories of faces. The ability of 12‐month‐olds to form separate child and infant categories suggests that they have a more exclusive representation of face age, one that may be influenced by prior experience with infant faces.     

Lecturers' faces fatigue their students: Face identity aftereffects for dynamic and static faces

Face adaptation has been used as a tool to probe our representations for facial identity. It has also been claimed to play a functional role in face processing, perhaps calibrating the visual system towards encountered faces. However, for this to be so, face aftereffects must be observable following adaptation to ecologically valid moving stimuli, not just after prolonged viewing of static images. We adapted our participants to videos, static image sequences or single images of the faces of lecturers who were personally familiar to them. All three stimulus types produced significant, and equivalent, face identity aftereffects, demonstrating that aftereffects are not confined to static images but can occur after exposure to more naturalistic stimuli. It is also further evidence against explanations of face adaptation effects solely in terms of low-level visual processing.     

Face encoding is not categorical: Consistent evidence across multiple types of contingent aftereffects

ABSTRACT

Race-contingent aftereffects indicate that faces of different races are encoded via dissociable visual channels. Race-contingent aftereffects reflect perceptions of typicality, indicating a gradual transition of activity across channels as faces change from looking more typical of one race to the other We examine whether faces forming more discrete categories (sex: male/female; species: human/monkey) are encoded in a similar fashion, or whether they are instead encoded via more dichotomous categorical judgements. Curves representing the rate of change of aftereffect magnitude as stimuli changed from male to female produced shallow slopes, closely resembling ratings of typicality, but differing significantly from slopes for categorical judgements. For species, aftereffect slopes were significantly shallower than both ratings of typicality and categorical judgements. Overall, these results suggest that the encoding of facial properties such as these is not categorical, but instead involves a graded response as stimulus typicality varies. Aftereffect slopes were similar across the two experiments, raising the possibility of a common system that is recruited during contingent adaptation, regardless of the specific dimension involved or the categories used by the experimenter.     

Atypical updating of face representations with experience in children with autism

Face identity aftereffects are significantly diminished in children with autism relative to typical children, which may reflect reduced perceptual updating with experience. Here, we investigated whether this atypicality also extends to non‐face stimulus categories, which might signal a pervasive visual processing difference in individuals with autism. We used a figural aftereffect task to measure directly perceptual updating following exposure to distorted upright faces, inverted faces and cars, in typical children and children with autism. A size‐change between study and test stimuli limited the likelihood that any processing atypicalities reflected group differences in adaptation to low‐level features of the stimuli. Results indicated that, relative to typical children, figural aftereffects for upright faces, but not inverted faces or cars, were significantly attenuated in children with autism. Moreover, the group difference was amplified when we isolated the ‘face‐selective’ component of the aftereffect, by partialling out the mid‐level shape adaptation common to upright and inverted face stimuli. Notably, the aftereffects of typical children were disproportionately larger for upright faces than for inverted faces and cars, but the magnitude of aftereffects of autistic children was not similarly modulated according to stimulus category. These findings are inconsistent with a pervasive adaptive coding atypicality relative to typical children, and suggest that reduced perceptual updating may constitute a high‐level, and possibly face‐selective, visual processing difference in children with autism.     

Opposite aftereffects for Chinese and Caucasian faces are selective for social category information and not just physical face differences

Opposite changes in perception (aftereffects) can be simultaneously induced for faces from different social categories—for example, Chinese and Caucasian faces. We investigated whether these aftereffects are generated in high-level face coding that is sensitive to the social category information in faces, or in earlier visual coding sensitive to simple physical differences between faces. We caricatured the race of face stimuli and created face continua ranging from caricatured Caucasian faces (SuperCaucasian) to caricatured Chinese faces (SuperChinese). Participants were adapted to oppositely distorted faces that were a fixed physical distance apart on the morph continua. Larger opposite aftereffects were found following adaptation to faces from different race categories (e.g., contracted Chinese and expanded Caucasian faces), than for faces that were the same physical distance apart on the morph continua, but were within a race category (e.g., contracted SuperChinese and expanded Chinese faces). These results suggest that opposite aftereffects for Chinese and Caucasian faces reflect the recalibration of face neurons tuned to high-level social category information.     

Opposite aftereffects for Chinese and Caucasian faces are selective for social category information and not just physical face differences

Opposite changes in perception (aftereffects) can be simultaneously induced for faces from different social categories—for example, Chinese and Caucasian faces. We investigated whether these aftereffects are generated in high-level face coding that is sensitive to the social category information in faces, or in earlier visual coding sensitive to simple physical differences between faces. We caricatured the race of face stimuli and created face continua ranging from caricatured Caucasian faces (SuperCaucasian) to caricatured Chinese faces (SuperChinese). Participants were adapted to oppositely distorted faces that were a fixed physical distance apart on the morph continua. Larger opposite aftereffects were found following adaptation to faces from different race categories (e.g., contracted Chinese and expanded Caucasian faces), than for faces that were the same physical distance apart on the morph continua, but were within a race category (e.g., contracted SuperChinese and expanded Chinese faces). These results suggest that opposite aftereffects for Chinese and Caucasian faces reflect the recalibration of face neurons tuned to high-level social category information.     

Perception and imagery of faces generate similar gender aftereffects

Visual adaptation is known to bias perception away from the properties of the adapting stimuli, toward opposite properties, resulting in perceptual aftereffects. For example, prolonged exposure to a face has been shown to produce an identity aftereffect, biasing perception of a subsequent face toward the opposite identity. Such repulsive aftereffects have been observed for both visually perceived and visually imagined faces, suggesting that both perception and imagery yield typical aftereffects. However, recent studies have reported opposite patterns of aftereffects for perception and imagery of face gender. In these studies, visually perceived faces produced typical effects in which perception of androgynous faces was biased away from the gender of the adaptor, whereas imagery of the same stimuli produced atypical aftereffects, biasing the perceived gender of androgynous faces toward the gender of the adaptor. These findings are highly unusual and warrant further research. The present study aimed to gather new evidence on the direction of gender aftereffects following perception and imagery of faces. Experiment 1 had participants view and imagine female and male faces of famous and non-famous individuals. To determine the effect of concomitant visual stimulation on imagery and adaptation, participants visualized faces both in the presence and in the absence of a visual input. In Experiment 2, participants were adapted to perceived and imagined faces of famous and non-famous actors matched on gender typicality. This manipulation allowed us to determine the effect of face familiarity on the magnitude of gender aftereffects. Contrary to evidence from previous studies, our results demonstrated that both perception and imagery produced typical aftereffects, biasing the perceived gender of androgynous faces in the opposite direction to the gender of the adaptor. Famous faces yielded largest adaptation effects across tasks. Experiment 2 confirmed that these effects depended on familiarity rather than on sexual dimorphism. In both experiments, this effect was greater for perception than imagery. Additionally, imagery of famous faces produced strongest aftereffects when it was performed in the absence of visual stimulation. The implications of these findings are discussed.     

Perceptual load influences auditory space perception in the ventriloquist aftereffect

A period of exposure to trains of simultaneous but spatially offset auditory and visual stimuli can induce a temporary shift in the perception of sound location. This phenomenon, known as the ‘ventriloquist aftereffect’, reflects a realignment of auditory and visual spatial representations such that they approach perceptual alignment despite their physical spatial discordance. Such dynamic changes to sensory representations are likely to underlie the brain’s ability to accommodate inter-sensory discordance produced by sensory errors (particularly in sound localization) and variability in sensory transduction. It is currently unknown, however, whether these plastic changes induced by adaptation to spatially disparate inputs occurs automatically or whether they are dependent on selectively attending to the visual or auditory stimuli. Here, we demonstrate that robust auditory spatial aftereffects can be induced even in the presence of a competing visual stimulus. Importantly, we found that when attention is directed to the competing stimuli, the pattern of aftereffects is altered. These results indicate that attention can modulate the ventriloquist aftereffect.     

Visual perception and visual mental imagery of emotional faces generate similar expression aftereffects

What is the relationship between visual perception and visual mental imagery of emotional faces? We investigated this question using a within-emotion perceptual adaptation paradigm in which adaptation to a strong version of an expression was paired with a test face displaying a weak version of the same emotion category. We predicted that within-emotion adaptation to perception and imagery of expressions would generate similar aftereffects, biasing perception of weak emotional test faces toward a more neutral value. Our findings confirmed this prediction. Adaptation to mental images yielded aftereffects that inhibited emotion recognition of test expressions, as participants were less accurate at recognising these stimuli compared to baseline. While the same inhibitory effect was observed when expressions were visually perceived, the size of the aftereffects was greater for perception than imagery. These findings suggest the existence of expression-selective neural mechanisms that subserve both visual perception and visual mental imagery of emotional faces.     

Probing the visual representation of faces with adaptation: A view from the other side of the mean

Sensory adaptation and visual aftereffects have long given insight into the neural codes underlying basic dimensions of visual perception. Recently discovered perceptual adaptation effects for complex shapes like faces can offer similar insight into high-level visual representations. In the experiments reported here, we demonstrated first that face adaptation transfers across a substantial change in viewpoint and that this transfer occurs via processes unlikely to be specific to faces. Next, we probed the visual codes underlying face recognition using face morphs that varied selectively in reflectance or shape. Adaptation to these morphs affected the perception of "opposite" faces both from the same viewpoint and from a different viewpoint. These results are consistent with high-level face representations that pool local shape and reflectance patterns into configurations that specify facial appearance over a range of three-dimensional viewpoints. These findings have implications for computational models of face recognition and for competing neural theories of face and object recognition.     

Opposite effects of visual versus imagined presentation of faces on subsequent sex perception

Viewing faces of one sex changes the perception of subsequently seen ambiguous faces. Here we investigate if the mechanisms responsible for this sex aftereffect are also activated during mental imagery of faces. Participants categorized the sex of ambiguous faces after either viewing images of male or female actors' faces or imagining these same faces. As in previous studies, the ambiguous images were categorized as female more often after viewing male faces than after viewing female faces. The opposite effect was found for imagined faces, however; the ambiguous images were categorized as female more often after imagining female faces than after imagining male faces. Although our results are inconsistent with findings that imagined faces cause either no aftereffects or similar aftereffects to visually presented faces, our results are consistent with recent evidence that visual and imagined presentation of faces cause opposite adaptation effects on an early electrophysiological response associated with face processing.     

Face adaptation in an isolated population of African hunter-gatherers: Exposure influences perception of other-ethnicity faces more than own-ethnicity faces

Previous experiments have demonstrated that exposure to faces can change the perception of normality in new faces, such that faces similar to those at exposure appear more normal. Here we examined how experience influences adaptation effects in African Hadza hunter-gatherers, who have limited experience with White faces. We exposed participants to sets of either Hadza or White European faces that were manipulated to possess either wide-spaced or narrow-spaced eyes. We collected normality judgments both pre-exposure and post-exposure by showing pairs of images, one with wide-spaced and one with narrow-spaced eyes. Examining the difference between the pre-exposure and post-exposure judgments revealed that participants selected an increased number of images that were congruent with the faces to which they had been exposed. The change in normality judgments was strongest for White faces, suggesting that representations of White ethnicity faces are more malleable and less robust to adaptation, potentially because of the decreased experience that individuals had with them. A second experiment using the same test stimuli with a sample of White participants revealed equivalent adaptation effects for both Hadza and White faces. These data highlight the role of experience on the high-level visual adaptation of faces.     

Face aftereffects indicate dissociable, but not distinct, coding of male and female faces

It has been claimed that exposure to distorted faces of one sex induces perceptual aftereffects for test faces that are of the same sex, but not for test faces of the other sex (A. C. Little, L. M. DeBruine, & B. C. Jones, 2005). This result suggests that male and female faces have separate neural coding. Given the high degree of visual similarity between faces of different sexes, this result is surprising. The authors reinvestigated male and female face coding using a different face distortion. In Experiment 1, participants adapted to distorted faces from one sex (e.g., male contracted faces) and were tested with faces of both sexes. Aftereffects were found for both male and female faces, suggesting the existence of common coding mechanisms. In Experiments 2 and 3, participants adapted to oppositely distorted faces from both sexes (male contracted and female expanded faces). Weak opposite aftereffects were found for male and female faces, suggesting the existence of sex-selective face coding mechanisms. Taken together, these results indicate that both common and sex-selective mechanisms code male and female faces.     

Not to be and then to be: visual representation of ignored unfamiliar faces

Negative priming, the increase in response time and/or errors to targets previously encountered as distractors, is explained by inhibitory mechanisms that block the access of distractor representations to response systems. The processing of unfamiliar human faces was investigated using negative priming. Observers viewed a row of faces to decide whether 2 target faces were the same or different. Response latencies were longer when 1 or both targets had appeared as distractors on the immediately preceding trial--evidence that never-before seen faces are represented and require inhibition. Response latencies were shorter when face targets had appeared as distractors, either corrupted with high-frequency noise or contrast inverted--evidence that representations are facilitated. Finally, response latencies remained unaltered when face targets had appeared as upside-down distractors--evidence that not all distractor representations afford response priming. The visual system indeed represents ignored unfamiliar faces, but blocks these representations only if they vie with targets for the control of action.     

Prism adaptation in left-handers

Two experiments with left-handers examined the features of prism adaptation established by previous research with right-handers. Regardless of handedness, (1) rapid adaptation occurs in exposure pointing with developing error in the opposite direction after target achievement, especially with early visual feedback in target pointing; (2) proprioceptive or visual aftereffects are larger, depending on whether visual feedback is available early or late, respectively, in target pointing; (3) the sum of these aftereffects is equal to the total aftereffect for the eye-hand coordination loop; (4) intermanual transfer of visual aftereffects occurs only for the dominant hand; and (5) visual aftereffects are larger in left space when the dominant hand is exposed to leftward displacement. A notable handedness difference is that, while transfer of proprioceptive aftereffects only occurs to the nondominant hand in right-handers, transfer occurs in both directions for left-handers, but regardless of handedness, such transfer only occurs when the exposed hand is tested first after exposure. A discussion then focuses on the implications of these data for a theory of handedness.     

Figural aftereffects in the perception of faces

We examined figural aftereffects in images of human faces, for which changes in configuration are highly discriminable. Observers either matched or rated faces before or after viewing distorted images of faces. Prior adaptation strongly biases face perception by causing the original face to appear distorted in a direction opposite to the adapting distortion. Aftereffects transferred across different faces and were similar for upright or inverted faces, but were weaker when the adapting and test faces had different orientations (e.g., adapt inverted and test upright). Thus the aftereffects depend on which images are distorted, and not simply on the type of distortion introduced. We further show that the aftereffects are asymmetric, for adapting to the original face has little effect on the perception of a distorted face. This asymmetry suggests that adaptation may play an important normalizing role in face perception. Our results suggest that in normal viewing, figural aftereffects may strongly influence form perception and could provide a novel method for probing properties of human face perception.     

Nature and nurture in own-race face processing

A standard visual preference task was used to examine 3-month-olds' looking times at own-race versus other-race faces as a function of environmental exposure to faces from the two categories. Participants were Caucasian infants living in a Caucasian environment, African infants living in an African environment, and African infants living in a predominantly Caucasian environment. The results indicate that preference for own-race faces is present as early as 3 months of age, but that this preference results from exposure to the prototypical facial environment.