Haptic face identification activates ventral occipital and temporal areas: an fMRI study

Many studies in visual face recognition have supported a special role for the right fusiform gyrus. Despite the fact that faces can also be recognized haptically, little is known about the neural correlates of haptic face recognition. In the current fMRI study, neurologically intact participants were intensively trained to identify specific facemasks (molded from live faces) and specific control objects. When these stimuli were presented in the scanner, facemasks activated left fusiform and right hippocampal/parahippocampal areas (and other regions) more than control objects, whereas the latter produced no activity greater than the facemasks. We conclude that these ventral occipital and temporal areas may play an important role in the haptic identification of faces at the subordinate level. We further speculate that left fusiform gyrus may be recruited more for facemasks than for control objects because of the increased need for sequential processing by the haptic system.     

A haptic face-inversion effect

We examined whether a face-inversion effect occurs when participants explore faces by touch. We used a haptic version of the inversion paradigm with 3-D clay facemasks and non-face control objects (teapots) moulded from real objects. Young, neurologically intact, blindfolded participants performed a temporally unconstrained haptic same/different task in each of four stimulus conditions: upright facemasks, inverted facemasks, upright teapots, and inverted teapots. There was a significant inversion effect for faces in terms of accuracy, but none for teapots. The results are considered in terms of the consequences of sequential manual exploration for haptic face processing.     

Early development of letter specialization in left fusiform is associated with better word reading and smaller fusiform face area

A functional region of left fusiform gyrus termed “the visual word form area” (VWFA) develops during reading acquisition to respond more strongly to printed words than to other visual stimuli. Here, we examined responses to letters among 5‐ and 6‐year‐old early kindergarten children (N = 48) with little or no school‐based reading instruction who varied in their reading ability. We used functional magnetic resonance imaging (fMRI) to measure responses to individual letters, false fonts, and faces in left and right fusiform gyri. We then evaluated whether signal change and size (spatial extent) of letter‐sensitive cortex (greater activation for letters versus faces) and letter‐specific cortex (greater activation for letters versus false fonts) in these regions related to (a) standardized measures of word‐reading ability and (b) signal change and size of face‐sensitive cortex (fusiform face area or FFA; greater activation for faces versus letters). Greater letter specificity, but not letter sensitivity, in left fusiform gyrus correlated positively with word reading scores. Across children, in the left fusiform gyrus, greater size of letter‐sensitive cortex correlated with lesser size of FFA. These findings are the first to suggest that in beginning readers, development of letter responsivity in left fusiform cortex is associated with both better reading ability and also a reduction of the size of left FFA that may result in right‐hemisphere dominance for face perception.     

Structure and function in acquired prosopagnosia: Lessons from a series of 10 patients with brain damage

Acquired prosopagnosia varies in both behavioural manifestations and the location and extent of underlying lesions. We studied 10 patients with adult‐onset lesions on a battery of face‐processing tests. Using signal detection methods, we found that discriminative power for the familiarity of famous faces was most reduced by bilateral occipitotemporal lesions that involved the fusiform gyri, and better preserved with unilateral right‐sided lesions. Tests of perception of facial structural configuration showed severe deficits with lesions that included the right fusiform gyrus, whether unilateral or bilateral. This deficit was most consistent for eye configuration, with some patients performing normally for mouth configuration. Patients with anterior temporal lesions had better configuration perception, though at least one patient showed a more subtle failure to integrate configural data from different facial regions. Facial imagery, an index of facial memories, was severely impaired by bilateral lesions that included the right anterior temporal lobe and marginally impaired by fusiform lesions alone; unilateral right fusiform lesions tended to spare imagery for facial features. These findings suggest that (1) prosopagnosia is more severe with bilateral than unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition, (2) perception of facial configuration critically involves the right fusiform gyrus and (3) access to facial memories is most disrupted by bilateral lesions that also include the right anterior temporal lobe. This supports assertions that more apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more associative variants are linked to anterior temporal damage. Next, we found that behavioural indices of covert recognition correlated with measures of overt familiarity, consistent with theories that covert behaviour emerges from the output of damaged neural networks, rather than alternative pathways. Finally, to probe the face specificity of the prosopagnosic defect, we tested recognition of fruits and vegetables: While face specificity was not found in most of our patients, the data of one patient suggested that this may be possible with more focal lesions of the right fusiform gyrus.     

Neural adaptation across viewpoint and exemplar in fusiform cortex

The visual system has the remarkable ability to generalize across different viewpoints and exemplars to recognize abstract categories of objects, and to discriminate between different viewpoints and exemplars to recognize specific instances of particular objects. Behavioral experiments indicate the critical role of the right hemisphere in specific-viewpoint and -exemplar visual form processing and the left hemisphere in abstract-viewpoint and -exemplar visual form processing. Neuroimaging studies indicate the role of fusiform cortex in these processes, however results conflict in their support of the behavioral findings. We investigated this inconsistency in the present study by examining adaptation across viewpoint and exemplar changes in the functionally defined fusiform face area (FFA) and in fusiform regions exhibiting adaptation. Subjects were adapted to particular views of common objects and then tested with objects appearing in four critical conditions: same-exemplar, same-viewpoint adapted, same-exemplar, different-viewpoint adapted, different-exemplar adapted, and not adapted. In line with previous results, the FFA demonstrated a release from neural adaptation for repeated different viewpoints and exemplars of an object. In contrast to previous work, a (non-FFA) right medial fusiform area also demonstrated a release from neural adaptation for repeated different viewpoints and exemplars of an object. Finally, a left lateral fusiform area demonstrated neural adaptation for repeated different viewpoints, but not exemplars, of an object. Test-phase task demands did not affect adaptation in these regions. Together, results suggest that dissociable neural subsystems in fusiform cortex support the specific identification of a particular object and the abstract recognition of that object observed from a different viewpoint. In addition, results suggest that areas within fusiform cortex do not support abstract recognition of different exemplars of objects within a category.     

Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information

Working memory for names and faces was investigated to ascertain whether verbal and nonspatial visual information is maintained in working memory by separate neural systems. The subjects performed a delayed match-to-sample task for famous or unfamous faces and names and a sensorimotor control task. Several occipital, temporal, parietal, and prefrontal areas were activated during all memory delays, in comparison with the control delays. Greater delay activity for unfamous faces than for names was obtained in the right fusiform gyrus, right inferior frontal gyrus (IFG), right IFG/ precentral gyrus, and right medial superior frontal gyrus, whereas greater delay activity for unfamous names than for faces was observed in the precuneus, left insula/postcentral gyrus, and left IFG/ precentral gyrus. There was no significant difference in the prefrontal activity in the comparison between famous faces and names. Greater delay activity for famous names than for faces was obtained in visual association and parietal areas. The results indicate that there is a functional dissociation based on information type within the neural system that is responsible for working memory maintenance of verbal and nonspatial visual information.     

Functional neuroimaging studies of category specificity in object recognition: a critical review and meta-analysis

Functional neuroimaging studies in which the cortical organization for semantic knowledge has been addressed have revealed interesting dissociations in the recognition of different object categories, such as faces, natural objects, and manufactured objects. The present paper critically reviews these studies and performs a meta-analysis of stereotactic coordinates to determine whether category membership predicts patterns of brain activation across different studies. This meta-analysis revealed that, in the ventral temporal cortex, recognition of manufactured objects activates more medial aspects of the fusiform gyrus, as compared with natural object or face recognition. Face recognition activates more inferior aspects of the ventral temporal cortex, as compared with manufactured object recognition. The recognition task used—viewing, matching, or naming—also predicted brain activation patterns. Specifically, matching tasks recruit more inferior occipital regions than do either naming or viewing tasks, whereas naming tasks recruit more anterior ventral temporal sites than do either viewing or matching tasks. These findings indicate that the cognitive demands of a particular recognition task are as predictive of cortical activation patterns as is category membership.     

Neural developmental changes in processing inverted faces

We explored developmental changes in neural substrates for face processing, using fMRI. Children and adults performed a perceptual-matching task with upright and inverted face and animal stimuli. Behaviorally, inversion disrupted face processing more than animal processing for adults and older children. In line with this behavioral pattern, the left middle occipital gyrus showed a stronger face than animal inversion effect in adults. Moreover, a superior aspect of this region showed a greater face inversion effect in older than in younger children, indicating a developmental change in the processing of inverted faces. The visual regions recruited for inverted face processing in adults also overlapped more with brain regions involved in the viewing of upright objects than with regions involved in the viewing of upright faces in an independent localizer task. Hence, when faces are inverted, adults recruit regions normally engaged for recognizing objects, possibly pointing to a role for the featural processing of inverted faces.     

TMS to the “occipital face area” affects recognition but not categorization of faces

The human cortical system for face perception is comprised of a network of connected regions including the middle fusiform gyrus (“fusiform face area” or FFA), the inferior occipital cortex (“occipital face area” or OFA), and the superior temporal sulcus. The traditional hierarchical feedforward model of visual processing suggests information flows from early visual cortex to the OFA for initial face feature analysis to higher order regions including the FFA for identity recognition. However, patient data suggest an alternative model. Patients with acquired prosopagnosia, an inability to visually recognize faces, have been documented with lesions to the OFA but who nevertheless show face-selective activation in the FFA. Moreover, their ability to categorize faces remains intact. This suggests that the FFA is not solely responsible for face recognition and the network is not strictly hierarchical, but may be organized in a reverse hierarchical fashion. We used transcranial magnetic stimulation (TMS) to temporarily disrupt processing in the OFA in neurologically-intact individuals and found participants’ ability to categorize intact versus scrambled faces was unaffected, however face identity discrimination was significantly impaired. This suggests that face categorization but not recognition can occur without the “earlier” OFA being online and indicates that “lower level” face category processing may be assumed by other intact face network regions such as the FFA. These results are consistent with the patient data and support a non-hierarchical, global-to-local model with re-entrant connections between the OFA and other face processing areas.     

Differential development of selectivity for faces and bodies in the fusiform gyrus

Viewing faces or bodies activates category‐selective areas of visual cortex, including the fusiform face area (FFA), fusiform body area (FBA), and extrastriate body area (EBA). Here, using fMRI, we investigate the development of these areas, focusing on the right FFA and FBA. Despite the overlap of functionally defined FFA and FBA (54%–75% overlap), we found that these regions developed along different trajectories. With age (7–32 years old), the FFA gradually increased in size and selectivity, and was significantly larger and more face‐selective in adults than children. By contrast, the size and selectivity of the FBA did not correlate with age, and were equivalent in children and adults. Whereas in adults the FFA and FBA were comparable in size, in children the FBA was on average 70% larger than the FFA. These findings suggest that, in children, the fusiform gyrus is predominantly selective for bodies, with commensurate face‐selective responses apparent later in development. Moreover, differences in the development of the FFA and FBA indicate that overlapping functional brain areas, supported by the same anatomical structure, can develop along different trajectories.     

双侧梭状回面孔区在面孔加工中的功能分工与协作

梭状回面孔区(fusiform face area,FFA)是视觉皮层上专门加工面孔的区域。然而,双侧FFA在面孔加工中的功能分工与协作还存在争议。在特异性刺激的加工上,右侧FFA主要负责人类面孔类别的知觉,而左侧FFA的功能与面孔精细特征的感知有关;在皮层可塑性上,右侧FFA主要参与青少年的社会适应学习,而左侧FFA负责成年人的知觉学习;在面孔网络中,二者与不同区域的连接用以适应不同的认知需求;他们之间的有向协作具有任务特定性。未来研究需要回答三个问题:左侧FFA的可塑性程度及这一可塑性是否是认知特定的、左侧FFA及其形成的网络连接的认知意义,双侧FFA在面孔网络中的连接有向性等问题。     

TMS to the “occipital face area” affects recognition but not categorization of faces

The human cortical system for face perception is comprised of a network of connected regions including the middle fusiform gyrus (“fusiform face area” or FFA), the inferior occipital cortex (“occipital face area” or OFA), and the superior temporal sulcus. The traditional hierarchical feedforward model of visual processing suggests information flows from early visual cortex to the OFA for initial face feature analysis to higher order regions including the FFA for identity recognition. However, patient data suggest an alternative model. Patients with acquired prosopagnosia, an inability to visually recognize faces, have been documented with lesions to the OFA but who nevertheless show face-selective activation in the FFA. Moreover, their ability to categorize faces remains intact. This suggests that the FFA is not solely responsible for face recognition and the network is not strictly hierarchical, but may be organized in a reverse hierarchical fashion. We used transcranial magnetic stimulation (TMS) to temporarily disrupt processing in the OFA in neurologically-intact individuals and found participants’ ability to categorize intact versus scrambled faces was unaffected, however face identity discrimination was significantly impaired. This suggests that face categorization but not recognition can occur without the “earlier” OFA being online and indicates that “lower level” face category processing may be assumed by other intact face network regions such as the FFA. These results are consistent with the patient data and support a non-hierarchical, global-to-local model with re-entrant connections between the OFA and other face processing areas.     

Voice recognition and the posterior cingulate: An fMRI study of prosopagnosia

Voices, in addition to faces, enable person identification. Voice recognition has been shown to evoke a distributed network of brain regions that includes, in addition to the superior temporal sulcus (STS), the anterior temporal pole, fusiform face area (FFA), and posterior cingulate gyrus (pCG). Here we report an individual (MS) with acquired prosopagnosia who, despite bilateral damage to much of this network, demonstrates the ability to distinguish voices of several well‐known acquaintances from voices of people that he has never heard before. Functional magnetic resonance imaging (fMRI) revealed that, relative to speech‐modulated noise, voices rated as familiar and unfamiliar by MS elicited enhanced haemodynamic activity in the left angular gyrus, left posterior STS, and posterior midline brain regions, including the retrosplenial cortex and the dorsal pCG. More interestingly, relative to noise and unfamiliar voices, the familiar voices elicited greater haemodynamic activity in the left angular gyrus and medial parietal regions including the dorsal pCG and precuneus. The findings are consistent with theories implicating the pCG in recognizing people who are personally familiar, and furthermore suggest that the pCG region of the voice identification network is able to make functional contributions to voice recognition even though other areas of the network, namely the anterior temporal poles, FFA, and the right parietal lobe, may be compromised.     

Can generic expertise explain special processing for faces?

Does face recognition involve face-specific cognitive and neural processes ('domain specificity') or do faces only seem special because people have had more experience of individuating them than they have of individuating members of other homogeneous object categories ('the expertise hypothesis')? Here, we summarize new data that test these hypotheses by assessing whether classic face-selective effects - holistic processing, recognition impairments in prosopagnosia and fusiform face area activation - remain face selective in comparison with objects of expertise. We argue that evidence strongly supports domain specificity rather than the expertise hypothesis. We conclude that the crucial social function of face recognition does not reflect merely a general practice phenomenon and that it might be supported by evolved mechanisms (visual or nonvisual) and/or a sensitive period in infancy.     

Self-face recognition is characterized by “bilateral gain” and by faster,more accurate performance which persists when faces are inverted

We examine interhemispheric cooperation in the recognition of personally known faces whose long-term familiarity ensures frequent co-activation of face-sensitive areas in the right and left brain. Images of self, friend, and stranger faces were presented for 150 ms in upright and inverted orientations both unilaterally, in the right or left visual field, and bilaterally. Consistent with previous research, we find a bilateral advantage for familiar but not for unfamiliar faces, and we demonstrate that this gain occurs for inverted as well as upright faces. We show that friend faces are recognized more quickly than unfamiliar faces in upright but not in inverted orientations, suggesting that configural processing underlies this particular advantage. Novel to this study is the finding that people are faster and more accurate at recognizing their own face over both stranger and friend faces and that these advantages occur for both upright and inverted faces. These findings are consistent with evidence for a bilateral representation of self-faces.     

Evidence for individual face discrimination in non-face selective areas of the visual cortex in acquired prosopagnosia

Two areas in the human occipito-temporal cortex respond preferentially to faces: 'the fusiform face area' ('FFA') and the 'occipital face area' ('OFA'). However, it is unclear whether these areas have an exclusive role in processing faces, or if sub-maximal responses in other visual areas such as the lateral occipital complex (LOC) are also involved. To clarify this issue, we tested a brain-damaged patient (PS) presenting a face-selective impairment with functional magnetic resonance imaging (fMRI). The right hemisphere lesion of the prosopagnosic patient encompasses the 'OFA' but preserves the 'FFA' and LOC. Using fMRI-adaptation, we found a larger response to different faces than repeated faces in the ventral part of the LOC both for normals and the patient, next to her right hemisphere lesion. This observation indicates that following prosopagnosia, areas that do not respond preferentially to faces such as the ventral part of the LOC (vLOC) may still be recruited to subtend residual perception of individual faces.     

Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis

A number of human brain areas showing a larger response to faces than to objects from different categories, or to scrambled faces, have been identified in neuroimaging studies. Depending on the statistical criteria used, the set of areas can be overextended or minimized, both at the local (size of areas) and global (number of areas) levels. Here we analyzed a whole-brain factorial functional localizer obtained in a large sample of right-handed participants (40). Faces (F), objects (O; cars) and their phase-scrambled counterparts (SF, SO) were presented in a block design during a one-back task that was well matched for difficulty across conditions. A conjunction contrast at the group level {(F-SF) and (F-O)} identified six clusters: in the pulvinar, inferior occipital gyrus (so-called OFA), middle fusiform gyrus (so-called FFA), posterior superior temporal sulcus, amygdala, and anterior infero-temporal cortex, which were all strongly right lateralized. While the FFA showed the largest difference between faces and cars, it also showed the least face-selective response, responding more to cars than scrambled cars. Moreover, the FFA's larger response to scrambled faces than scrambled cars suggests that its face-sensitivity is partly due to low-level visual cues. In contrast, the pattern of activation in the OFA points to a higher degree of face-selectivity. A BOLD latency mapping analysis suggests that face-sensitivity emerges first in the right FFA, as compared to all other areas. Individual brain analyses support these observations, but also highlight the large amount of interindividual variability in terms of number, height, extent and localization of the areas responding preferentially to faces in the human ventral occipito-temporal cortex. This observation emphasizes the need to rely on different statistical thresholds across the whole brain and across individuals to define these areas, but also raises some concerns regarding any objective labeling of these areas to make them correspond across individual brains. This large-scale analysis helps understanding the set of face-sensitive areas in the human brain, and encourages in-depth single participant analyses in which the whole set of areas is considered in each individual brain.     

Where you look can influence haptic object recognition

We investigated whether the relative position of objects and the body would influence haptic recognition. People felt objects on the right or left side of their body midline, using their right hand. Their head was turned towards or away from the object, and they could not see their hands or the object. People were better at naming 2-D raised line drawings and 3-D small-scale models of objects and also real, everyday objects when they looked towards them. However, this head-towards benefit was reliable only when their right hand crossed their body midline to feel objects on their left side. Thus, haptic object recognition was influenced by people's head position, although vision of their hand and the object was blocked. This benefit of turning the head towards the object being explored suggests that proprioceptive and haptic inputs are remapped into an external coordinate system and that this remapping is harder when the body is in an unusual position (with the hand crossing the body midline and the head turned away from the hand). The results indicate that haptic processes align sensory inputs from the hand and head even though either hand-centered or object-centered coordinate systems should suffice for haptic object recognition.     

Hemispheric asymmetry in cross-race face recognition

This study examines two phenomena related to face perception, both of which depend on experience and holistic processing: perceivers process faces more efficiently in the right hemisphere of the brain (a hemispheric asymmetry), and they typically show greater recognition accuracy for members of their racial ingroup (a cross-race recognition deficit). The current study tests the possibility that these two effects are related. If asymmetry depends on experience, it should be particularly evident with (more familiar) ingroup faces; if cross-race recognition relies on holistic processing, it should be particularly evident for faces presented to the right hemisphere. Black and White participants viewed Black and White faces presented to either the left or right visual field. As predicted, participants showed a more pronounced asymmetry for ingroup (rather than outgroup) faces, and cross-race recognition deficits were more pronounced for stimuli presented to the left (rather than the right) visual field.