Holistic processing of the mouth but not the eyes in developmental prosopagnosia

Because holistic processing is a hallmark of normal face recognition, we ask whether such processing is reduced in developmental prosopagnosia (DP), and, if so, what the sources are of this deficit. Existing literature provides a mixed picture, with face inversion effects showing consistent holistic processing deficits but unable to locate their source and with some composite face studies showing reduced holistic processing and some not. We addressed this issue more thoroughly with a very large sample of DPs (N = 38) performing the part–whole task, a well-accepted measure of holistic processing that allows for the separate evaluation of individual face parts. Contrary to an expected overall reduction in holistic processing, we found an intact holistic advantage for the mouth and a complete absence of a holistic advantage for the eye region. Less severely impaired prosopagnosics showed significantly more holistic processing of the mouth, suggesting that holistic processing can aid them in recognizing faces.     

The spatial frequency spectrum of fearful faces modulates early and mid-latency ERPs but not the N170

Prioritized processing of fearful compared to neutral faces is reflected in behavioral advantages such as lower detection thresholds, but also in enhanced early and late event-related potentials (ERPs). Behavioral advantages have recently been associated with the spatial frequency spectrum of fearful faces, better fitting the human contrast sensitivity function than the spectrum of neutral faces. However, it is unclear whether and to which extent early and late ERP differences are due to low-level spatial frequency spectrum information or high-level representations of the facial expression. In this pre-registered EEG study (N = 38), the effects of fearful-specific spatial frequencies on event-related ERPs were investigated by presenting faces with fearful and neutral expressions whose spatial frequency spectra were manipulated so as to contain either the average power spectra of neutral, fearful, or both expressions combined. We found an enlarged N170 to fearful versus neutral faces, not interacting with spatial frequency. Interactions of emotional expression and spatial frequencies were observed for the P1 and Early Posterior Negativity (EPN). For both components, larger emotion differences were observed when the spectrum contained neutral as opposed to fearful frequencies. Importantly, for the EPN, fearful and neutral expressions did not differ anymore when inserting fearful frequencies into neutral expressions, whereas typical emotion differences were found when faces contained average or neutral frequencies. Our findings show that N170 emotional modulations are unaffected by expression-specific spatial frequencies. However, expression-specific spatial frequencies alter early and mid-latency ERPs. Most notably, the EPN to neutral expressions is boosted by adding fearful spectra—but not vice versa.     

Topographic processing in developmental prosopagnosia: Preserved perception but impaired memory of scenes

Anecdotal evidence suggests a relation between impaired spatial (navigational) processing and developmental prosopagnosia. To address this formally, we tested two aspects of topographic processing – that is, perception and memory of mountain landscapes shown from different viewpoints. Participants included nine individuals with developmental prosopagnosia and 18 matched controls. The group with developmental prosopagnosia had no difficulty with topographic perception, but was reliably poorer in the retention of topographic information. Additional testing revealed that this did not reflect a general deficit in visual processing or visual short-term memory. Interestingly, a classical dissociation could be demonstrated between impaired face memory and preserved topographic memory in two developmental prosopagnosics. We conclude that impairments in topographic memory tend to co-occur with developmental prosopagnosia, although the underlying functions are likely to be independent.     

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.     

Naso-temporal asymmetry for signals invisible to the retinotectal pathway

Monocular viewing conditions show an asymmetry between stimuli presented in the temporal and nasal visual fields in their efficiency for automatically triggering eye saccades and grasping attention. For instance, observers free to make a saccade to one of two stimuli presented together orient preferentially to the temporal stimulus. Such naso-temporal asymmetry (NTA) has been assumed to reflect the asymmetry in the retinotectal pathway to the superior colliculus. We tested this hypothesis using S cone stimuli, which are invisible to the magnocellular and retinotectal pathways. The observed NTA in choice saccades to bilateral stimuli was no less present for S cone stimuli than for luminance stimuli. Additionally, the amplitude of the NTA can be enhanced when S cone signals are added to luminance signals. These results suggest that behavioral NTA in humans is not diagnostic of retinotectal mediation. Furthermore, we found no asymmetries in latency, suggesting that the NTA in saccade choice does not originate simply from a bottom-up asymmetry in any low level visual pathways.     

Configural processing of other-race faces is delayed but not decreased

The processing of other-race faces has been suggested to differ from own-race face processing with regard to the extent to which configural and/or holistic information is taken into account. We aimed at investigating the underlying mechanisms more precisely by applying event-related potentials (ERP). We presented upright and inverted own-race, other-race, and other-species faces (apes), as well as non-facial control stimuli (houses), and analysed the effects of stimulus type and inversion on the N170. Peak latencies for same-race, other-race, other-species, and non-face stimuli gradually increased, and inversion of all types of face stimuli led to an additional delay. Importantly, the two factors did not interact for face stimuli. Inversion increased N170 amplitudes for own- and other-race faces only. We conclude that early perceptual mechanisms of face processing are not qualitatively different for own- and other-race faces. Instead, the same underlying processes appear to work less efficiently for other-race faces.     

Face recognition impairments despite normal holistic processing and face space coding: Evidence from a case of developmental prosopagnosia

Holistic processing and face space coding are widely considered primary perceptual mechanisms behind good face recognition. Here, however, we present the case of S.P., a developmental prosopagnosic who demonstrated severe impairments in face memory and face perception, yet showed normal holistic processing and face space coding. Across three composite experiments, S.P. showed normal-strength holistic processing for upright faces and no composite effect for inverted faces. Across five aftereffect experiments, S.P. showed normal-sized face aftereffects, which derived normally from face space rather than shape-generic mechanisms. The case of S.P. implies: (a) normal holistic processing and face space coding can be insufficient for good face recognition even when present in combination; and (b) the focus of recent literature on holistic processing and face space should be expanded to include other potential face processing mechanisms (e.g., part-based processing). Our article also highlights the importance of internal task reliability in drawing inferences from single-case studies.     

Electrophysiological studies of face processing in developmental prosopagnosia: Neuropsychological and neurodevelopmental perspectives

People with developmental prosopagnosia (DP) show severe face-recognition deficits that typically emerge during childhood without history of neurological damage. We review findings from recent event-related brain potential (ERP) studies of face perception and face recognition in DP. The generic face-sensitivity of the N170 component is present in most DPs, suggesting rapid category-selective streaming of facial information. In contrast, DPs show atypical N170 face inversion effects, indicative of impaired structural encoding, specifically for upright faces. In line with neurodevelopmental accounts of DP, these effects are similar to those observed for other developmental disorders, as well as for younger children and older adults. Identity-sensitive ERP components (N250, P600f) triggered during successful face recognition are similar for DPs and control participants, indicating that the same mechanisms are active in both groups. The presence of covert face-recognition effects for the N250 component suggests that visual face memory and semantic memory can become disconnected in some individuals with DP. The implications of these results for neuropsychological and neurodevelopmental perspectives on DP are discussed.     

Modification of N170 by different emotional expression of schematic faces

The N170 is widely regarded as a face sensitive potential, having its maximum at occipito-temporal sites, with right-hemisphere dominance. However, it is debatable whether the N170 is modulated by different emotional expressions of a face. The aim of this study was to analyze the N170 elicited by schematic happy and angry faces when the emotional expression is semantically processed. To investigate the influence of different emotional expressions of schematic faces, we used a Prime-Probe procedure with the N400 effect as an indicator for a semantic processing. Eighteen subjects were presented the German word "happiness" or "anger" followed by happy and angry faces. The word-face pair could be congruent or incongruent in emotional meaning. Subjects were instructed to compare the emotional meaning of the words and faces and to count the congruent trials. Event-related potentials were recorded from 124 sites. Congruent faces elicited a smaller negativity in the N400 time range than incongruent faces, indicating that the facial emotional expression was cognitively processed. The face sensitive N170 was most pronounced at posterior and occipital sites, and N170 amplitudes were larger following the angry as compared to the happy faces. It is concluded that different emotional expressions of schematic faces can modulate the N170.     

Face recognition impairments despite normal holistic processing and face space coding: evidence from a case of developmental prosopagnosia

Holistic processing and face space coding are widely considered primary perceptual mechanisms behind good face recognition. Here, however, we present the case of S.P., a developmental prosopagnosic who demonstrated severe impairments in face memory and face perception, yet showed normal holistic processing and face space coding. Across three composite experiments, S.P. showed normal-strength holistic processing for upright faces and no composite effect for inverted faces. Across five aftereffect experiments, S.P. showed normal-sized face aftereffects, which derived normally from face space rather than shape-generic mechanisms. The case of S.P. implies: (a) normal holistic processing and face space coding can be insufficient for good face recognition even when present in combination; and (b) the focus of recent literature on holistic processing and face space should be expanded to include other potential face processing mechanisms (e.g., part-based processing). Our article also highlights the importance of internal task reliability in drawing inferences from single-case studies.     

Evidence for anatomical but not functional asymmetry in the hemidecorticate rat

Rats with unilateral ablation of the left or right cerebral neocortex or left or right hippocampus were studied in a battery of tests of spatial orientation, motor coordination, and social behavior, including Morris water task, radial arm maze, feeding, narrow beam traversing, puzzle latches, hoarding, grooming, nest building, running wheel activity, male--male interaction, and shock-induced aggression. Comparison of the brains of operated and control rats confirmed previous suggestions that the right hemisphere of the rat is bigger and may have different connections than the left hemisphere. Despite the morphological asymmetries, comparison of the behavior of rats with right hemidecortication with that of rats with left hemidecortication, and of rats with right and of those with left hippocampal lesions, failed to show a single instance of functional asymmetry in the rat brain. These behavioral results stand in marked contrast to previous reports of functional asymmetry in the control of activity, orientation, and rotation.     

Delayed processing of global shape information is associated with weaker top-down effects in developmental prosopagnosia

ABSTRACT

In previous studies we have shown that a group of individuals with developmental prosopagnosia (DP): (i) were impaired at recognizing objects when presented as silhouettes or fragmented forms; stimuli which place particular demands on global shape processing, (ii) that these impairments correlated with their face recognition deficit, (iii) that they showed a reduced global precedence effect in Navon’s paradigm, and (iv) that the magnitude of their global precedence effect correlated with their face and object recognition performance. This pattern of deficits points towards a delay in the processing of global shape information; a delay that may weaken top-down influences on recognition performance. Here we show that the DPs show reduced real object superiority effects (faster responses to real objects than nonobjects) compared with controls. Given that real object superiority effects reflect top-down processing, these findings support the notion of impaired global shape based top-down processing in DP.     

Right N170 modulation in a face discrimination task: an account for categorical perception of familiar faces

Behavioral studies have shown that two different morphed faces belonging to the same identity are harder to discriminate than two faces stemming from two different identities. The temporal course of this categorical perception effect has been explored through event-related potentials. Three kinds of pairs were presented in a matching task: (1) two different morphed faces representing the same identity (within), (2) two other faces representing two different identities (between), and (3) two identical morphed faces (same). Following the second face onset in the pair, the amplitude of the right occipitotemporal negativity (N170) was reduced for within and same pairs as compared with between pairs, suggesting an identity priming effect. We also observed a modulation of the P3b wave, as the amplitude of the responses for within pairs was higher than for between and same pairs, suggesting a higher complexity of the task for within pairs. These results indicate that categorical perception of human faces has a perceptual origin in the right occipitotemporal hemisphere.     

Scan patterns during the processing of facial identity in prosopagnosia

The scan patterns of ocular fixations made by prosopagnosic patients while they attempt to identify faces may provide insights into how they process the information in faces. Contrasts between their scanning of upright versus inverted faces may index the presence of a hypothesized orientation-dependent expert mechanism for processing faces, while contrasts between their scanning of familiar versus novel faces may index the influence of residual facial memories on their search for meaningful facial information. We recorded the eye movements of two prosopagnosics while they viewed faces. One patient, with acquired prosopagnosia from a right occipitotemporal lesion, showed degraded orientation effects but still with a normal distribution of fixations to more salient facial features. However, the dynamics of his global scan patterns were more chaotic for novel faces, suggesting degradation of an internal facial schema, and consistent with other evidence of impaired face configuration perception in this patient. His global scan patterns for famous faces differed from novel faces, suggesting the influence of residual facial memories, as indexed previously by his relatively good imagery for famous faces. The other patient, with a developmental prosopagnosia, showed anomalous orientation effects, abnormal distribution of fixations to less salient regions, and chaotic global scan patterns, in keeping with a more severe loss of face-expert mechanisms. The effects of fame on her scanning were weaker than those in the first subject and non-existent in her global scan patterns. We conclude that scan patterns in prosopagnosia can both reflect the loss of orientation-dependent expert mechanisms and index the covert influence of residual facial memories. In these two subjects the scanning data were consistent with other results from tests of configuration perception, imagery, and covert recognition.     

A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia

Whether the ability to recognize facial expression can be preserved in the absence of the recognition of facial identity remains controversial. The current study reports the results of a detailed investigation of facial expression recognition in three congenital prosopagnosic (CP) participants, in comparison with two patients with acquired prosopagnosia (AP) and a large group of 30 neurologically normal participants, including individually age- and gender-matched controls. Participants completed a fine-grained expression recognition paradigm requiring a six-alternative forced-choice response to continua of morphs of six different basic facial expressions (e.g. happiness and surprise). Accuracy, sensitivity and reaction times were measured. The performance of all three CP individuals was indistinguishable from that of controls, even for the most subtle expressions. In contrast, both individuals with AP displayed pronounced difficulties with the majority of expressions. The results from the CP participants attest to the dissociability of the processing of facial identity and of facial expression. Whether this remarkably good expression recognition is achieved through normal, or compensatory, mechanisms remains to be determined. Either way, this normal level of performance does not extend to include facial identity.     

The overlap of neural selectivity between faces and words: evidences from the N170 adaptation effect

Faces and words both evoke an N170, a strong electrophysiological response that is often used as a marker for the early stages of expert pattern perception. We examine the relationship of neural selectivity between faces and words by using a novel application of cross-category adaptation to the N170. We report a strong asymmetry between N170 adaptation induced by faces and by words. This is the first electrophysiological result showing that neural selectivity to faces encompasses neural selectivity to words and suggests that the N170 response to faces constitutes a neural marker for versatile representations of familiar visual patterns.     

Effects of level of processing but not of task enactment on recognition memory in a case of developmental amnesia

We report the performance in four recognition memory experiments of Jon, a young adult with early-onset developmental amnesia whose episodic memory is gravely impaired in tests of recall, but seems relatively preserved in tests of recognition, and who has developed normal levels of performance in tests of intelligence and general knowledge. Jon's recognition performance was enhanced by deeper levels of processing in comparing a more meaningful study task with a less meaningful one, but not by task enactment in comparing performance of an action with reading an action phrase. Both of these variables normally enhance episodic remembering, which Jon claimed to experience. But Jon was unable to support that claim by recollecting what it was that he remembered. Taken altogether, the findings strongly imply that Jon's recognition performance entailed little genuine episodic remembering and that the levels-of-processing effects in Jon reflected semantic, not episodic, memory.     

Effects of level of processing but not of task enactment on recognition memory in a case of developmental amnesia

We report the performance in four recognition memory experiments of Jon, a young adult with early-onset developmental amnesia whose episodic memory is gravely impaired in tests of recall, but seems relatively preserved in tests of recognition, and who has developed normal levels of performance in tests of intelligence and general knowledge. Jon's recognition performance was enhanced by deeper levels of processing in comparing a more meaningful study task with a less meaningful one, but not by task enactment in comparing performance of an action with reading an action phrase. Both of these variables normally enhance episodic remembering, which Jon claimed to experience. But Jon was unable to support that claim by recollecting what it was that he remembered. Taken altogether, the findings strongly imply that Jon's recognition performance entailed little genuine episodic remembering and that the levels-of-processing effects in Jon reflected semantic, not episodic, memory.     

Specificity of impaired facial identity recognition in children with suspected developmental prosopagnosia

Adults experiencing face recognition difficulties in the absence of known brain injury are described as cases of developmental prosopagnosia (DP), under the assumption that specific face recognition impairments have always been present. However, only five childhood cases of DP have been reported, and the majority had additional socio-communicative impairments consistent with an autism spectrum disorder (ASD). We tested face recognition skills of six 4- to 8-year-old children, who were suspected of having DP, and tested for ASD using established diagnostic tools. Two children met criteria for ASD. One child did not exhibit consistent face recognition impairments. The remaining three children were severely impaired on multiple tasks of unfamiliar face recognition despite normal cognitive functioning and no evidence of ASD. Two of these children were also impaired at object recognition suggesting more general visual recognition problems. The final child showed normal object recognition demonstrating apparently specific problems with facial identity recognition.