Introducing the female Cambridge face memory test - long form (F-CFMT+).

The Cambridge Face Memory Test (CFMT) is one of the most used assessments of face recognition abilities in the science of face processing. The original task, using White male faces, has been empirically evaluated for psychometric properties (Duchaine & Nakayama, 2006), while the longer and more difficult version (CFMT+; Russell et al., 2009) has not. Critically, no version exists using female faces. Here, we present the Female Cambridge Face Memory Test - Long Form (F-CFMT+) and evaluate the psychometric properties of this task in comparison to the Male Cambridge Face Memory Test - Long Form (M-CFMT+). We tested typically developing emerging adults (18 to 25 years old) in both Cambridge face recognition tasks, an old-new face recognition task, and a car recognition task. Results indicate that the F-CFMT+ is a valid, internally consistent measure of unfamiliar face recognition that can be used alone or in tandem with the M-CFMT+ to assess recognition abilities for young adult White faces. When used together, performance on the F-CFMT+ and M-CFMT+ can be directly compared, adding to the ability to understand face recognition abilities for different kinds of faces. The two tasks have high convergent validity and relatively good divergent validity with car recognition in the same task paradigm. The F-CFMT+ will be useful to researchers interested in evaluating a broad range of questions about face recognition abilities in both typically developing individuals and those with atypical social information processing abilities.

The Oxford Face Matching Test: A non-biased test of the full range of individual differences in face perception.

Tests of face processing are typically designed to identify individuals performing outside of the typical range; either prosopagnosic individuals who exhibit poor face processing ability, or super recognisers, who have superior face processing abilities. Here we describe the development of the Oxford Face Matching Test (OFMT), designed to identify individual differences in face processing across the full range of performance, from prosopagnosia, through the range of typical performance, to super recognisers. Such a test requires items of varying difficulty, but establishing difficulty is problematic when particular populations (e.g., prosopagnosics, individuals with autism spectrum disorder) may use atypical strategies to process faces. If item difficulty is calibrated on neurotypical individuals, then the test may be poorly calibrated for atypical groups, and vice versa. To obtain items of varying difficulty, we used facial recognition algorithms to obtain face pair similarity ratings that are not biased towards specific populations. These face pairs were used as stimuli in the OFMT, and participants were required to judge whether the face images depicted the same individual or different individuals. Across five studies the OFMT was shown to be sensitive to individual differences in the typical population, and in groups of both prosopagnosic individuals and super recognisers. The test-retest reliability of the task was at least equivalent to the Cambridge Face Memory Test and the Glasgow Face Matching Test. Furthermore, results reveal, at least at the group level, that both face perception and face memory are poor in those with prosopagnosia, and are good in super recognisers.

Attentional modulation differentially affects ventral and dorsal face areas in both normal participants and developmental prosopagnosics.

Face-selective cortical areas that can be divided into a ventral stream and a dorsal stream. Previous findings indicate selective attention to particular aspects of faces have different effects on the two streams. To better understand the organization of the face network and whether deficits in attentional modulation contribute to developmental prosopagnosia (DP), we assessed the effect of selective attention to different face aspects across eight face-selective areas. Our results from normal participants found that ROIs in the ventral pathway (OFA, FFA) responded strongly when attention was directed to identity and expression, and ROIs in the dorsal pathway (pSTS-FA, IFG-FA) responded the most when attention was directed to facial expression. Response profiles generated by attention to different face aspects were comparable in DPs and normals. Our results demonstrate attentional modulation affects the ventral and dorsal steam face areas differently and indicate deficits in attentional modulation do not contribute to DP.

Using High Frequency Transcranial Random Noise Stimulation to Modulate Face Memory Performance in Younger and Older Adults: Lessons Learnt From Mixed Findings.

High-frequency transcranial random noise stimulation (tRNS) has been shown to improve a range of cognitive and perceptual abilities. Here we sought to examine the effects of a single session of tRNS targeted at the ventrolateral prefrontal cortices (VLPFC) on face memory in younger and older adults. To do so, we conducted three experiments. In Experiment 1, we found that younger adults receiving active tRNS outperformed those receiving sham stimulation (i.e., using a between-participant factor for stimulation condition; Experiment 1). This effect was not observed for object memory (car memory) in younger adults (Experiment 2), indicating that the effect is not a general memory effect. In Experiment 3, we sought to replicate the effects of Experiment 1 using a different design (within-participant factor of stimulation - active or sham tRNS to the same individual) and to extend the study by including older adult participants. In contrast to Experiment 1, we found that active tRNS relative to sham tRNS reduced face memory performance in both younger and older adults. We also found that the degree of decline in performance in the active tRNS relative to sham tRNS condition was predicted by baseline ability, with higher performing participants showing the largest decreases in performance. Overall, the results indicate that tRNS to the VLPFC modulates face memory, but that there may be performance and protocol specific moderators of this effect. We discuss these findings in the context of the broader literature showing the importance of individual variation in the outcome of non-invasive brain stimulation intervention approaches. We conclude that while tRNS may have potential as an intervention approach, generalizing from single experiment studies to wide application is risky and caution should be adopted in interpreting findings.

Developmental prosopagnosics have widespread selectivity reductions across category-selective visual cortex.

Developmental prosopagnosia (DP) is a neurodevelopmental disorder characterized by severe deficits with facial identity recognition. It is unclear which cortical areas contribute to face processing deficits in DP, and no previous studies have investigated whether other category-selective areas function normally in DP. To address these issues, we scanned 22 DPs and 27 controls using a dynamic localizer consisting of video clips of faces, scenes, bodies, objects, and scrambled objects. We then analyzed category selectivity, a measure of the tuning of a cortical area to a particular visual category. DPs exhibited reduced face selectivity in all 12 face areas, and the reductions were significant in three posterior and two anterior areas. DPs and controls showed similar responses to faces in other category-selective areas, which suggests the DPs' behavioral deficits with faces result from problems restricted to the face network. DPs also had pronounced scene-selectivity reductions in four of six scene-selective areas and marginal body-selectivity reductions in two of four body-selective areas. Our results demonstrate that DPs have widespread deficits throughout the face network, and they are inconsistent with a leading account of DP which proposes that posterior face-selective areas are normal in DP. The selectivity reductions in other category-selective areas indicate many DPs have deficits spread across high-level visual cortex.

Normal composite face effects in developmental prosopagnosia.

Upright face perception is thought to involve holistic processing, whereby local features are integrated into a unified whole. Consistent with this view, the top half of one face appears to fuse perceptually with the bottom half of another, when aligned spatially and presented upright. This 'composite face effect' reveals a tendency to integrate information from disparate regions when faces are presented canonically. In recent years, the relationship between susceptibility to the composite effect and face recognition ability has received extensive attention both in participants with normal face recognition and participants with developmental prosopagnosia. Previous results suggest that individuals with developmental prosopagnosia may show reduced susceptibility to the effect suggestive of diminished holistic face processing. Here we describe two studies that examine whether developmental prosopagnosia is associated with reduced composite face effects. Despite using independent samples of developmental prosopagnosics and different composite procedures, we find no evidence for reduced composite face effects. The experiments yielded similar results; highly significant composite effects in both prosopagnosic groups that were similar in magnitude to the effects found in participants with normal face processing. The composite face effects exhibited by both samples and the controls were greatly diminished when stimulus arrangements were inverted. Our finding that the whole-face binding process indexed by the composite effect is intact in developmental prosopagnosia indicates that other factors are responsible for developmental prosopagnosia. These results are also inconsistent with suggestions that susceptibility to the composite face effect and face recognition ability are tightly linked. While the holistic process revealed by the composite face effect may be necessary for typical face perception, it is not sufficient; individual differences in face recognition ability likely reflect variability in multiple sequential processes.

Normal voice processing after posterior superior temporal sulcus lesion.

The right posterior superior temporal sulcus (pSTS) shows a strong response to voices, but the cognitive processes generating this response are unclear. One possibility is that this activity reflects basic voice processing. However, several fMRI and magnetoencephalography findings suggest instead that pSTS serves as an integrative hub that combines voice and face information. Here we investigate whether right pSTS contributes to basic voice processing by testing Faith, a patient whose right pSTS was resected, with eight behavioral tasks assessing voice identity perception and recognition, voice sex perception, and voice expression perception. Faith performed normally on all the tasks. Her normal performance indicates right pSTS is not necessary for intact voice recognition and suggests that pSTS activations to voices reflect higher-level processes.

Face Processing Systems: From Neurons to Real-World Social Perception.

Primate face processing depends on a distributed network of interlinked face-selective areas composed of face-selective neurons. In both humans and macaques, the network is divided into a ventral stream and a dorsal stream, and the functional similarities of the areas in humans and macaques indicate they are homologous. Neural correlates for face detection, holistic processing, face space, and other key properties of human face processing have been identified at the single neuron level, and studies providing causal evidence have established firmly that face-selective brain areas are central to face processing. These mechanisms give rise to our highly accurate familiar face recognition but also to our error-prone performance with unfamiliar faces. This limitation of the face system has important implications for consequential situations such as eyewitness identification and policing.

Effective Connectivity from Early Visual Cortex to Posterior Occipitotemporal Face Areas Supports Face Selectivity and Predicts Developmental Prosopagnosia.

Face processing is mediated by interactions between functional areas in the occipital and temporal lobe, and the fusiform face area (FFA) and anterior temporal lobe play key roles in the recognition of facial identity. Individuals with developmental prosopagnosia (DP), a lifelong face recognition impairment, have been shown to have structural and functional neuronal alterations in these areas. The present study investigated how face selectivity is generated in participants with normal face processing, and how functional abnormalities associated with DP, arise as a function of network connectivity. Using functional magnetic resonance imaging and dynamic causal modeling, we examined effective connectivity in normal participants by assessing network models that include early visual cortex (EVC) and face-selective areas and then investigated the integrity of this connectivity in participants with DP. Results showed that a feedforward architecture from EVC to the occipital face area, EVC to FFA, and EVC to posterior superior temporal sulcus (pSTS) best explained how face selectivity arises in both controls and participants with DP. In this architecture, the DP group showed reduced connection strengths on feedforward connections carrying face information from EVC to FFA and EVC to pSTS. These altered network dynamics in DP contribute to the diminished face selectivity in the posterior occipitotemporal areas affected in DP. These findings suggest a novel view on the relevance of feedforward projection from EVC to posterior occipitotemporal face areas in generating cortical face selectivity and differences in face recognition ability. SIGNIFICANCE STATEMENT: Areas of the human brain showing enhanced activation to faces compared to other objects or places have been extensively studied. However, the factors leading to this face selectively have remained mostly unknown. We show that effective connectivity from early visual cortex to posterior occipitotemporal face areas gives rise to face selectivity. Furthermore, people with developmental prosopagnosia, a lifelong face recognition impairment, have reduced face selectivity in the posterior occipitotemporal face areas and left anterior temporal lobe. We show that this reduced face selectivity can be predicted by effective connectivity from early visual cortex to posterior occipitotemporal face areas. This study presents the first network-based account of how face selectivity arises in the human brain.

The Anterior Temporal Face Area Contains Invariant Representations of Face Identity That Can Persist Despite the Loss of Right FFA and OFA.

Macaque neurophysiology found image-invariant representations of face identity in a face-selective patch in anterior temporal cortex. A face-selective area in human anterior temporal lobe (fATL) has been reported, but has not been reliably identified, and its function and relationship with posterior face areas is poorly understood. Here, we used fMRI adaptation and neuropsychology to ask whether fATL contains image-invariant representations of face identity, and if so, whether these representations require normal functioning of fusiform face area (FFA) and occipital face area (OFA). We first used a dynamic localizer to demonstrate that 14 of 16 normal subjects exhibit a highly selective right fATL. Next, we found evidence that this area subserves image-invariant representation of identity: Right fATL showed repetition suppression to the same identity across different images, while other areas did not. Finally, to examine fATL's relationship with posterior areas, we used the same procedures with Galen, an acquired prosopagnosic who lost right FFA and OFA. Despite the absence of posterior face areas, Galen's right fATL preserved its face selectivity and showed repetition suppression comparable to that in controls. Our findings suggest that right fATL contains image-invariant face representations that can persist despite the absence of right FFA and OFA, but these representations are not sufficient for normal face recognition.

Normal perception of Mooney faces in developmental prosopagnosia: Evidence from the N170 component and rapid neural adaptation.

Individuals with developmental prosopagnosia (DP) have a severe difficulty recognizing the faces of known individuals in the absence of any history of neurological damage. These recognition problems may be linked to selective deficits in the holistic/configural processing of faces. We used two-tone Mooney images to study the processing of faces versus non-face objects in DP when it is based on holistic information (or the facial gestalt) in the absence of obvious local cues about facial features. A rapid adaptation procedure was employed for a group of 16 DPs. Naturalistic photographs of upright faces were preceded by upright or inverted Mooney faces or by Mooney houses. DPs showed face-sensitive N170 components in response to Mooney faces versus houses, and N170 amplitude reductions for inverted as compared to upright Mooney faces. They also showed the typical pattern of N170 adaptation effects, with reduced N170 components when upright naturalistic test faces were preceded by upright Mooney faces, demonstrating that the perception of Mooney and naturalistic faces recruits shared neural populations. Our findings demonstrate that individuals with DP can utilize global information about face configurations for categorical discriminations between faces and non-face objects, and suggest that face processing deficits emerge primarily at more fine-grained higher level stages of face perception.

Local but not long-range microstructural differences of the ventral temporal cortex in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DP) experience face recognition impairments despite normal intellect and low-level vision and no history of brain damage. Prior studies using diffusion tensor imaging in small samples of subjects with DP (n=6 or n=8) offer conflicting views on the neurobiological bases for DP, with one suggesting white matter differences in two major long-range tracts running through the temporal cortex, and another suggesting white matter differences confined to fibers local to ventral temporal face-specific functional regions of interest (fROIs) in the fusiform gyrus. Here, we address these inconsistent findings using a comprehensive set of analyzes in a sample of DP subjects larger than both prior studies combined (n=16). While we found no microstructural differences in long-range tracts between DP and age-matched control participants, we found differences local to face-specific fROIs, and relationships between these microstructural measures with face recognition ability. We conclude that subtle differences in local rather than long-range tracts in the ventral temporal lobe are more likely associated with developmental prosopagnosia.

Acquired prosopagnosia without word recognition deficits.

It has long been suggested that face recognition relies on specialized mechanisms that are not involved in visual recognition of other object categories, including those that require expert, fine-grained discrimination at the exemplar level such as written words. But according to the recently proposed many-to-many theory of object recognition (MTMT), visual recognition of faces and words are carried out by common mechanisms [Behrmann, M., & Plaut, D. C. ( 2013 ). Distributed circuits, not circumscribed centers, mediate visual recognition. Trends in Cognitive Sciences, 17, 210-219]. MTMT acknowledges that face and word recognition are lateralized, but posits that the mechanisms that predominantly carry out face recognition still contribute to word recognition and vice versa. MTMT makes a key prediction, namely that acquired prosopagnosics should exhibit some measure of word recognition deficits. We tested this prediction by assessing written word recognition in five acquired prosopagnosic patients. Four patients had lesions limited to the right hemisphere while one had bilateral lesions with more pronounced lesions in the right hemisphere. The patients completed a total of seven word recognition tasks: two lexical decision tasks and five reading aloud tasks totalling more than 1200 trials. The performances of the four older patients (3 female, age range 50-64 years) were compared to those of 12 older controls (8 female, age range 56-66 years), while the performances of the younger prosopagnosic (male, 31 years) were compared to those of 14 younger controls (9 female, age range 20-33 years). We analysed all results at the single-patient level using Crawford's t-test. Across seven tasks, four prosopagnosics performed as quickly and accurately as controls. Our results demonstrate that acquired prosopagnosia can exist without word recognition deficits. These findings are inconsistent with a key prediction of MTMT. They instead support the hypothesis that face recognition is carried out by specialized mechanisms that do not contribute to recognition of written words.

High-Frequency Transcranial Random Noise Stimulation Enhances Perception of Facial Identity.

Recently, a number of studies have demonstrated the utility of transcranial current stimulation as a tool to facilitate a variety of cognitive and perceptual abilities. Few studies, though, have examined the utility of this approach for the processing of social information. Here, we conducted 2 experiments to explore whether a single session of high-frequency transcranial random noise stimulation (tRNS) targeted at lateral occipitotemporal cortices would enhance facial identity perception. In Experiment 1, participants received 20 min of active high-frequency tRNS or sham stimulation prior to completing the tasks examining facial identity perception or trustworthiness perception. Active high-frequency tRNS facilitated facial identity perception, but not trustworthiness perception. Experiment 2 assessed the spatial specificity of this effect by delivering 20 min of active high-frequency tRNS to lateral occipitotemporal cortices or sensorimotor cortices prior to participants completing the same facial identity perception task used in Experiment 1. High-frequency tRNS targeted at lateral occipitotemporal cortices enhanced performance relative to motor cortex stimulation. These findings show that high-frequency tRNS to lateral occipitotemporal cortices produces task-specific and site-specific enhancements in face perception.

Normal body perception despite the loss of right fusiform gyrus.

Human extrastriate cortex contains functional regions that are selective for particular categories such as faces, bodies, and places, but it is unclear whether these category-selective regions are necessary for normal perception of their preferred stimuli. One of these regions is the right fusiform body area (FBA), which is selectively involved in body perception. Do loss of the right fusiform gyrus and the absence of the right FBA necessarily lead to deficits in body perception? Here we report the performance of Galen, a brain-damaged patient who lost the right fusiform gyrus and has no right FBA, on eight tasks of body perception. Despite his lesion, Galen showed normal performance on all tasks. Galen's results demonstrate that damage to the right fusiform gyrus and the lack of the right FBA do not necessarily lead to persisting deficits in body perception.

Combined TMS and FMRI reveal dissociable cortical pathways for dynamic and static face perception.

Faces contain structural information, for identifying individuals, as well as changeable information, which can convey emotion and direct attention. Neuroimaging studies reveal brain regions that exhibit preferential responses to invariant [1, 2] or changeable [3-5] facial aspects but the functional connections between these regions are unknown. We addressed this issue by causally disrupting two face-selective regions with thetaburst transcranial magnetic stimulation (TBS) and measuring the effects of this disruption in local and remote face-selective regions with functional magnetic resonance imaging (fMRI). Participants were scanned, over two sessions, while viewing dynamic or static faces and objects. During these sessions, TBS was delivered over the right occipital face area (rOFA) or right posterior superior temporal sulcus (rpSTS). Disruption of the rOFA reduced the neural response to both static and dynamic faces in the downstream face-selective region in the fusiform gyrus. In contrast, the response to dynamic and static faces was doubly dissociated in the rpSTS. Namely, disruption of the rOFA reduced the response to static but not dynamic faces, while disruption of the rpSTS itself reduced the response to dynamic but not static faces. These results suggest that dynamic and static facial aspects are processed via dissociable cortical pathways that begin in early visual cortex, a conclusion inconsistent with current models of face perception [6-9].

Normal acquisition of expertise with greebles in two cases of acquired prosopagnosia.

Face recognition is generally thought to rely on different neurocognitive mechanisms than most types of objects, but the specificity of these mechanisms is debated. One account suggests the mechanisms are specific to upright faces, whereas the expertise view proposes the mechanisms operate on objects of high within-class similarity with which an observer has become proficient at rapid individuation. Much of the evidence cited in support of the expertise view comes from laboratory-based training experiments involving computer-generated objects called greebles that are designed to place face-like demands on recognition mechanisms. A fundamental prediction of the expertise hypothesis is that recognition deficits with faces will be accompanied by deficits with objects of expertise. Here we present two cases of acquired prosopagnosia, Herschel and Florence, who violate this prediction: Both show normal performance in a standard greeble training procedure, along with severe deficits on a matched face training procedure. Herschel and Florence also meet several response time criteria that advocates of the expertise view suggest signal successful acquisition of greeble expertise. Furthermore, Herschel's results show that greeble learning can occur without normal functioning of the right fusiform face area, an area proposed to mediate greeble expertise. The marked dissociation between face and greeble expertise undermines greeble-based claims challenging face-specificity and indicates face recognition mechanisms are not necessary for object recognition after laboratory-based training.

Intranasal inhalation of oxytocin improves face processing in developmental prosopagnosia.

Developmental prosopagnosia (DP) is characterised by a severe lifelong impairment in face recognition. In recent years it has become clear that DP affects a substantial number of people, yet little work has attempted to improve face processing in these individuals. Intriguingly, recent evidence suggests that intranasal inhalation of the hormone oxytocin can improve face processing in unimpaired participants, and we investigated whether similar findings might be noted in DP. Ten adults with DP and 10 matched controls were tested using a randomized placebo-controlled double-blind within-subject experimental design (AB-BA). Each participant took part in two testing sessions separated by a 14-25 day interval. In each session, participants inhaled 24 IU of oxytocin or placebo spray, followed by a 45 min resting period to allow central oxytocin levels to plateau. Participants then completed two face processing tests: one assessing memory for a set of newly encoded faces, and one measuring the ability to match simultaneously presented faces according to identity. Participants completed the Multidimensional Mood Questionnaire (MMQ) at three points in each testing session to assess the possible mood-altering effects of oxytocin and to control for attention and wakefulness. Statistical comparisons revealed an improvement for DP but not control participants on both tests in the oxytocin condition, and analysis of scores on the MMQ indicated that the effect cannot be attributed to changes in mood, attention or wakefulness. This investigation provides the first evidence that oxytocin can improve face processing in DP, and the potential neural underpinnings of the findings are discussed alongside their implications for the treatment of face processing disorders.

The composite effect for inverted faces is reliable at large sample sizes and requires the basic face configuration.

The absence of the face composite effect (FCE) for inverted faces is often considered evidence that holistic processing operates only on upright faces. However, such absence might be explained by power issues: Most studies that have failed to find the inverted FCE tested 24 participants or less. Here we find that the inverted FCE exists reliably when we tested at least 60 participants. The inverted FCE was ∼ 18% the size of the upright FCE, and it was unaffected by testing order: It did not matter whether participants did the upright condition first (Experiment 1, n = 64) or the inverted condition first (Experiment 2, n = 68). The effect also remained when upright and inverted trials were mixed (Experiment 3, n = 60). An individual differences analysis found a modest positive correlation between inverted and upright FCE, suggesting partially shared mechanisms. A critical control experiment demonstrates that the inverted FCE cannot be explained by visuospatial attention or other generic accounts because the effect disappeared when the basic face configuration was disrupted (Experiment 4, n = 50). Our study shows that the inverted FCE is a reliable effect that requires an intact face configuration, consistent with the notion that some holistic processing also operates on inverted faces.