Lúcia Garrido

Transcranial Magnetic Stimulation Disrupts the Perception and Embodiment of Facial Expressions

Theories of embodied cognition propose that recognizing facial expressions requires visual processing followed by simulation of the somatovisceral responses associated with the perceived expression. To test this proposal, we targeted the right occipital face area (rOFA) and the face region of right somatosensory cortex (rSC) with repetitive transcranial magnetic stimulation (rTMS) while participants discriminated facial expressions. rTMS selectively impaired discrimination of facial expressions at both sites but had no effect on a matched face identity task. Site specificity within the rSC was demonstrated by targeting rTMS at the face and finger regions while participants performed the expression discrimination task. rTMS targeted at the face region impaired task performance relative to rTMS targeted at the finger region. To establish the temporal course of visual and somatosensory contributions to expression processing, double-pulse TMS was delivered at different times to rOFA and rSC during expression discrimination. Accuracy dropped when pulses were delivered at 60–100 ms at rOFA and at 100–140 and 130–170 ms at rSC. These sequential impairments at rOFA and rSC support embodied accounts of expression recognition as well as hierarchical models of face processing. The results also demonstrate that nonvisual cortical areas contribute during early stages of expression processing.

Voxel-based morphometry reveals reduced grey matter volume in the temporal cortex of developmental prosopagnosics

Individuals with developmental prosopagnosia exhibit severe and lasting difficulties in recognizing faces despite the absence of apparent brain abnormalities. We used voxel-based morphometry to investigate whether developmental prosopagnosics show subtle neuroanatomical differences from controls. An analysis based on segmentation of T1-weighted images from 17 developmental prosopagnosics and 18 matched controls revealed that they had reduced grey matter volume in the right anterior inferior temporal lobe and in the superior temporal sulcus/middle temporal gyrus bilaterally. In addition, a voxel-based morphometry analysis based on the segmentation of magnetization transfer parameter maps showed that developmental prosopagnosics also had reduced grey matter volume in the right middle fusiform gyrus and the inferior temporal gyrus. Multiple regression analyses relating three distinct behavioural component scores, derived from a principal component analysis, to grey matter volume revealed an association between a component related to facial identity and grey matter volume in the left superior temporal sulcus/middle temporal gyrus plus the right middle fusiform gyrus/inferior temporal gyrus. Grey matter volume in the lateral occipital cortex was associated with component scores related to object recognition tasks. Our results demonstrate that developmental prosopagnosics have reduced grey matter volume in several regions known to respond selectively to faces and provide new evidence that integrity of these areas relates to face recognition ability.

Deep and superficial amygdala nuclei projections revealed in vivo by probabilistic tractography.

Despite a homogenous macroscopic appearance on magnetic resonance images, subregions of the amygdala express distinct functional profiles as well as corresponding differences in connectivity. In particular, histological analysis shows stronger connections for superficial (i.e., centromedial and cortical), compared with deep (i.e., basolateral and other), amygdala nuclei to lateral orbitofrontal cortex and stronger connections of deep compared with superficial, nuclei to polymodal areas in the temporal pole. Here, we use diffusion weighted imaging with probabilistic tractography to investigate these connections in humans. We use a data-driven approach to segment the amygdala into two subregions using k-means clustering. The identified subregions are spatially contiguous and their location corresponds to deep and superficial nuclear groups. Quantification of the connection strength between these amygdala clusters and individual target regions corresponds to qualitative histological findings in non-human primates, indicating such findings can be extrapolated to humans. We propose that connectivity profiles provide a potentially powerful approach for in vivo amygdala parcellation and can serve as a guide in studies that exploit functional and anatomical neuroimaging.

Developmental phonagnosia: A selective deficit of vocal identity recognition

Phonagnosia, the inability to recognize familiar voices, has been studied in brain-damaged patients but no cases due to developmental problems have been reported. Here we describe the case of KH, a 60-year-old active professional woman who reports that she has always experienced severe voice recognition difficulties. Her hearing abilities are normal, and an MRI scan showed no evidence of brain damage in regions associated with voice or auditory perception. To better understand her condition and to assess models of voice and high-level auditory processing, we tested KH on behavioural tasks measuring voice recognition, recognition of vocal emotions, face recognition, speech perception, and processing of environmental sounds and music. KH was impaired on tasks requiring the recognition of famous voices and the learning and recognition of new voices. In contrast, she performed well on nearly all other tasks. Her case is the first report of developmental phonagnosia, and the results suggest that the recognition of a speakers vocal identity depends on separable mechanisms from those used to recognize other information from the voice or non-vocal auditory stimuli.

Face detection in normal and prosopagnosic individuals

Face detection, the process of finding a face in a visual scene, is a critical step in face processing, yet it has received relatively little attention compared with other face processes. The present study addresses this crucial first stage by investigating the effect of inversion on face detection and by examining how individuals with developmental prosopagnosia perform on face detection tasks. Fourteen control participants and fourteen individuals with developmental prosopagnosia (DPs) were tested with two face detection tasks: (I) Face versus Non-Face, where arrays of small images were presented, one of which could contain a face and (2) Face versus Face Parts, where a two-tone face could be embedded in a larger array of similar two-tone face parts. On each trial, participants made a speeded response if a face was present in the visual display. On almost all measures both normal and prosopagnosic individuals showed strong inversion effects with significantly worse performance with inverted faces. This shows that the simple task of detection can show inversion effects comparable to those seen for other face tasks, including recognition. Finally, while there were prosopagnosics who were well within the normal range for detection, there were significant group differences, particularly for the case of the Face versus Face Parts, where prosopagnosics were worse than controls on upright but not on inverted face detection.

Social anhedonia is associated with neural abnormalities during face emotion processing.

Human beings are social organisms with an intrinsic desire to seek and participate in social interactions. Social anhedonia is a personality trait characterized by a reduced desire for social affiliation and reduced pleasure derived from interpersonal interactions. Abnormally high levels of social anhedonia prospectively predict the development of schizophrenia and contribute to poorer outcomes for schizophrenia patients. Despite the strong association between social anhedonia and schizophrenia, the neural mechanisms that underlie individual differences in social anhedonia have not been studied and are thus poorly understood. Deficits in face emotion recognition are related to poorer social outcomes in schizophrenia, and it has been suggested that face emotion recognition deficits may be a behavioral marker for schizophrenia liability. In the current study, we used functional magnetic resonance imaging (fMRI) to see whether there are differences in the brain networks underlying basic face emotion processing in a community sample of individuals low vs. high in social anhedonia. We isolated the neural mechanisms related to face emotion processing by comparing face emotion discrimination with four other baseline conditions (identity discrimination of emotional faces, identity discrimination of neutral faces, object discrimination, and pattern discrimination). Results showed a group (high/low social anhedonia) × condition (emotion discrimination/control condition) interaction in the anterior portion of the rostral medial prefrontal cortex, right superior temporal gyrus, and left somatosensory cortex. As predicted, high (relative to low) social anhedonia participants showed less neural activity in face emotion processing regions during emotion discrimination as compared to each control condition. The findings suggest that social anhedonia is associated with abnormalities in networks responsible for basic processes associated with social cognition, and provide a starting point for understanding the neural basis of social motivation and our drive to seek social affiliation.

Superior Facial Expression, But Not Identity Recognition, in Mirror-Touch Synesthesia

Simulation models of expression recognition contend that to understand anothers facial expressions, individuals map the perceived expression onto the same sensorimotor representations that are active during the experience of the perceived emotion. To investigate this view, the present study examines facial expression and identity recognition abilities in a rare group of participants who show facilitated sensorimotor simulation (mirror-touch synesthetes). Mirror-touch synesthetes experience touch on their own body when observing touch to another person. These experiences have been linked to heightened sensorimotor simulation in the shared-touch network (brain regions active during the passive observation and experience of touch). Mirror-touch synesthetes outperformed nonsynesthetic participants on measures of facial expression recognition, but not on control measures of face memory or facial identity perception. These findings imply a role for sensorimotor simulation processes in the recognition of facial affect, but not facial identity.

Normal social cognition in developmental prosopagnosia

Face perception provides information critical to cognitive computations about the social world. This raises the possibility that the development of mechanisms used for social cognition may depend on the presence of normal face perception mechanisms, and this notion partly motivates an aetiological model of autism spectrum disorder (ASD) that suggests that deficits in face perception lead to the social cognition impairments that characterize ASD. To investigate these issues, we examined social cognition in participants with developmental prosopagnosia (DP). A total of 2 male DPs with severe facial identity and facial expression deficits showed no signs of impaired social cognition on three measures. A total of 10 other DPs responded to an inventory measuring autistic traits, and all except one performed normally. These results indicate that social cognition mechanisms can develop normally in the context of developmental face-processing impairments.

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.

Dissociation between face perception and face memory in adults, but not children, with developmental prosopagnosia

Highlights • Individuals with developmental prosopagnosia (DP) have impaired face recognition.• In theory, DP could involve impaired face memory, impaired face perception, or both.• Memory deficits were present in all of our child and adult DPs.• All children, but less than half of the adults had impaired face perception.