Thomas Busigny

Holistic perception of the individual face is specific and necessary : evidence from an extensive case study of acquired prosopagnosia

We present an extensive investigation (24 experiments) of a new case of prosopagnosia following right unilateral damage, GG, with the aim of addressing two classical issues: (1) Can a visual recognition impairment truly be specific to faces? (2) What is the nature of acquired prosopagnosia? We show that GG recognizes nonface objects perfectly and quickly, even when it requires fine-grained analysis to individualize these objects. He is also capable of perceiving objects and faces as integrated wholes, as indicated by normal Navon effect, 3D-figures perception and perception of Mooney and Arcimboldo face stimuli. However, the patient could not perceive individual faces holistically, showing no inversion, composite, or whole-part advantage effects for faces. We conclude that an occipito-temporal right hemisphere lesion may lead to a specific impairment of holistic perception of individual items, a function that appears critical for normal face recognition but not for object recognition.

Impaired holistic processing of unfamiliar individual faces in acquired prosopagnosia.

Prosopagnosia is an impairment at individualizing faces that classically follows brain damage. Several studies have reported observations supporting an impairment of holistic/configural face processing in acquired prosopagnosia. However, this issue may require more compelling evidence as the cases reported were generally patients suffering from integrative visual agnosia, and the sensitivity of the paradigms used to measure holistic/configural face processing in normal individuals remains unclear. Here we tested a well-characterized case of acquired prosopagnosia (PS) with no object recognition impairment, in five behavioral experiments (whole/part and composite face paradigms with unfamiliar faces). In all experiments, for normal observers we found that processing of a given facial feature was affected by the location and identity of the other features in a whole face configuration. In contrast, the patients results over these experiments indicate that she encodes local facial information independently of the other features embedded in the whole facial context. These observations and a survey of the literature indicate that abnormal holistic processing of the individual face may be a characteristic hallmark of prosopagnosia following brain damage, perhaps with various degrees of severity.

Holistic Face Categorization in Higher Order Visual Areas of the Normal and Prosopagnosic Brain: Toward a Non-Hierarchical View of Face Perception

How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (two-tones Mooney figures and Arcimboldos facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus (“Fusiform face area”) and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no “occipital face area”). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex.

Acquired prosopagnosia abolishes the face inversion effect

Individual faces are notoriously difficult to recognize when they are presented upside-down. Since acquired prosopagnosia (AP) has been associated with an impairment of expert face processes, a reduced or abolished face inversion effect (FIE) is expected in AP. However, previous studies have incongruently reported apparent normal effects of inversion, a decreased or abolished FIE, but also a surprisingly better performance for inverted faces for some patients. While these discrepant observations may be due to the variability of high-level processes impaired, a careful look at the literature rather suggests that the pattern of FIE in prosopagnosia has been obscured by a selection of patients with associated low-level defects and general visual recognition impairments, as well as trade-offs between accuracy and correct RT measures. Here we conducted an extensive investigation of upright and inverted face processing in a well-characterized case of face-selective AP, PS (Rossion et al., 2003). In 4 individual face discrimination experiments, PS did not present any inversion effect at all, taking into account all dependent measures of performance. However, she showed a small inversion cost for individualizing members of a category of non-face objects (cars), just like normal observers. A fifth experiment with personally familiar faces to recognize confirmed the lack of inversion effect for PS. Following the present report and a survey of the literature, we conclude that the FIE is generally absent, or at least clearly reduced following AP. We also suggest that the paradoxical superior performance for inverted faces observed in rare cases may be due to additional upper visual field defects rather than to high-level competing visual processes. These observations are entirely compatible with the view that AP is associated with a disruption of a process that is also abolished following inversion: the holistic representation of individual exemplars of the face class.

Acquired prosopagnosia as a face-specific disorder: Ruling out the general visual similarity account

Prosopagnosia is classically defined as a disorder of visual recognition specific to faces, following brain damage. However, according to a long-standing alternative view, these patients would rather be generally impaired in recognizing objects belonging to visually homogenous categories, including faces. We tested this alternative hypothesis stringently with a well-documented brain-damaged prosopagnosic patient (PS) in three delayed forced-choice recognition experiments in which visual similarity between a target and its distractor was manipulated parametrically: novel 3D geometric shapes, morphed pictures of common objects, and morphed photographs of a highly homogenous familiar category (cars). In all experiments, PS showed normal performance and speed, and there was no evidence of a steeper increase of error rates and RTs with increasing levels of visual similarity, compared to controls. These data rule out an account of acquired prosopagnosia in terms of a more general impairment in recognizing objects from visually homogenous categories. An additional experiment with morphed faces confirmed that PS was specifically impaired at individual face recognition. However, in stark contrast to the alternative view of prosopagnosia, PS was relatively more impaired at the easiest levels of discrimination, i.e. when individual faces differ clearly in global shape rather than when faces were highly similar and had to be discriminated based on fine-grained details. Overall, these observations as well as a review of previous evidence, lead us to conclude that this alternative view of prosopagnosia does not hold. Rather, it seems that brain damage in adulthood may lead to selective recognition impairment for faces, perhaps the only category of visual stimuli for which holistic/configural perception is not only potentially at play, but is strictly necessary to individualize members of the category efficiently.

Face-specific impairment in holistic perception following focal lesion of the right anterior temporal lobe.

Recent studies have provided solid evidence for pure cases of prosopagnosia following brain damage. The patients reported so far have posterior lesions encompassing either or both the right inferior occipital cortex and fusiform gyrus, and exhibit a critical impairment in generating a sufficiently detailed holistic percept to individualize faces. Here, we extended these observations to include the prosopagnosic patient LR (Bukach, Bub, Gauthier, & Tarr, 2006), whose damage is restricted to the anterior region of the right temporal lobe. First, we report that LR is able to discriminate parametrically defined individual exemplars of nonface object categories as accurately and quickly as typical observers, which suggests that the visual similarity account of prosopagnosia does not explain his impairments. Then, we show that LR does not present with the typical face inversion effect, whole-part advantage, or composite face effect and, therefore, has impaired holistic perception of individual faces. Moreover, the patient is more impaired at matching faces when the facial part he fixates is masked than when it is selectively revealed by means of gaze contingency. Altogether these observations support the view that the nature of the critical face impairment does not differ qualitatively across patients with acquired prosopagnosia, regardless of the localization of brain damage: all these patients appear to be impaired to some extent at what constitutes the heart of our visual expertise with faces, namely holistic perception at a sufficiently fine-grained level of resolution to discriminate exemplars of the face class efficiently. This conclusion raises issues regarding the existing criteria for diagnosis/classification of patients as cases of apperceptive or associative prosopagnosia.

Right anterior temporal lobe atrophy and person-based semantic defect: A detailed case study

We report a new case of a right temporal pole variant of frontotemporal dementia (Rtv-FTLD), MD, who presented a slowly progressive deterioration of the recognition of familiar and famous people. We thoroughly investigated MDs face processing and semantic abilities, including a neuroimaging investigation. This analysis revealed a cross-modal person-based deficit together with a more general semantic alteration. However, there was no evidence of impairment in face perception, including holistic processing, or of an abnormal pattern of brain activation in face-sensitive cortical areas. We discuss the nature of face processing in the Rtv-FTLD and the context of a person-based semantic defect.

Impairment of holistic face perception following right occipito-temporal damage in prosopagnosia : converging evidence from gaze-contingency

Gaze-contingency is a method traditionally used to investigate the perceptual span in reading by selectively revealing/masking a portion of the visual field in real time. Introducing this approach in face perception research showed that the performance pattern of a brain-damaged patient with acquired prosopagnosia (PS) in a face matching task was reversed, as compared to normal observers: the patient showed almost no further decrease of performance when only one facial part (eye, mouth, nose, etc.) was available at a time (foveal window condition, forcing part-based analysis), but a very large impairment when the fixated part was selectively masked (mask condition, promoting holistic perception) (Van Belle, De Graef, Verfaillie, Busigny, & Rossion, 2010a; Van Belle, De Graef, Verfaillie, Rossion, & Lefèvre, 2010b). Here we tested the same manipulation in a recently reported case of pure prosopagnosia (GG) with unilateral right hemisphere damage (Busigny, Joubert, Felician, Ceccaldi, & Rossion, 2010). Contrary to normal observers, GG was also significantly more impaired with a mask than with a window, demonstrating impairment with holistic face perception. Together with our previous study, these observations support a generalized account of acquired prosopagnosia as a critical impairment of holistic (individual) face perception, implying that this function is a key element of normal human face recognition. Furthermore, the similar behavioral pattern of the two patients despite different lesion localizations supports a distributed network view of the neural face processing structures, suggesting that the key function of human face processing, namely holistic perception of individual faces, requires the activity of several brain areas of the right hemisphere and their mutual connectivity.

Holistic processing impairment can be restricted to faces in acquired prosopagnosia : evidence from the global/local Navon effect

Previous studies have shown that acquired prosopagnosia is characterized by impairment at holistic/configural processing. However, this view is essentially supported by studies performed with patients whose face recognition difficulties are part of a more general visual (integrative) agnosia. Here, we tested the patient PS, a case of acquired prosopagnosia whose face-specific recognition difficulties have been related to the inability to process individual faces holistically (absence of inversion, composite, and whole-part effects with faces). Here, we show that in contrast to this impairment, the patient presents with an entirely normal response profile in a Navon hierarchical letter task: she was as fast as normal controls, faster to identify global than local letters, and her sensitivity to global interference during identification of local letters was at least as large as normal observers. These observations indicate that holistic processing as measured with global/local interference in the Navon paradigm is functionally distinct from the ability to perceive an individual face holistically.

A systematic study of topographical memory and posterior cerebral artery infarctions

Objective: To estimate the prevalence of topographical memory impairment following posterior cerebral artery infarctions (PCAI) and define its anatomical correlations. Methods: We recruited 15 patients (mean duration of 4 months postinfarct). We administered 2 sets of experimental tests to assess topographical memory: one set included 5 computerized tasks (CompT) and the other set consisted of one ecological topographical orientation test (EcolT) that included 4 tasks (i.e., map drawing, picture recognition and ordering, backward path). Fifteen healthy participants served as controls. Patients and controls underwent a volumetric T1 MRI brain scan. Brain lesions in patients were segmented, normalized, and correlated with performance. Results: Topographical memory impairments were evidenced in patients with PCAI using both group and individual analyses (50%), with more severe outcomes in patients with PCAI in the right hemisphere. CompT and EcolT were highly correlated, but the ecological test was more sensitive in revealing topographical memory impairments. Voxel-based lesion-symptom mapping demonstrated that 2 regions located in the cuneus and the calcarine sulcus correlated significantly with behavioral performance. Conclusions: Topographical memory disorders following PCAI are reported in 50% of the patient population. Our results demonstrate the importance of developing and using dedicated batteries of topographical memory tests, in particular real-life tests, to identify such deficits.