Introduction: Face-identity recognition is crucial for human communication and is likely based on a hierarchical process, initiated by face perception, followed by face-identity recognition and semantic association (Bruce & Young, 1986). At the neural level, this maps to cognitive models proposing a core-face and extended network that interact to support recognition. Posterior core-face regions process face perception (occipital face area: OFA; posterior fusiform face area: pFFA) and anterior regions (anterior FFA: aFFA; anterior temporal lobe face area: aTL-FA) familiar face-identity recognition. The extended network supports semantic association. Developmental prosopagnosia (DP) is a disorder marked by profound difficulties in recognizing faces, even highly familiar faces, in the absence of brain injury. To date, there is limited consensus regarding the underlying neural mechanisms of the disorder. Behavioral evidence highlights heterogeneity in DP, implying potential subtypes - apperceptive DP with face perception deficits, and associative DP with intact face perception, but difficulty recognizing familiar faces. Here, we applied a functional magnetic resonance imaging (fMRI) design with natural ambient images of familiar and unfamiliar faces to investigate and contrast the neural mechanisms of familiar and unfamiliar face-identity recognition in typically developed (TD) individuals and DPs who were meticulously characterized into potential behavioral subtypes. Hypotheses: Based on the hierarchical model of face-identity processing we predicted: H1) TD individuals recruit anterior core-face regions (aTL-FA and aFFA) during familiar face-identity processing and posterior core-face regions (OFA and pFFA) during unfamiliar face-identity processing. H2) DP individuals can be characterized into distinct behavioral phenotypes, i.e., apperceptive and associative subtypes, based on performance in face perception and face memory tasks. H3) The behavioral subtypes of DP are reflected in distinct neural response profiles: apperceptive DPs show overall reduced responses in all core-face regions to familiar and unfamiliar faces, while associative DPs show intact responses in posterior core-face regions, but reduced recruitment of anterior regions. Methods: To examine the core-face and extended network, functional imaging data was acquired using a multi-echo gradient echo planar imaging sequence optimized to image regions susceptible to signal drop-out, including the aTL, during the performance of a face-identity recognition task. In total, we recruited 33 TD and 18 DP participants. Before the fMRI task, DP cases were behaviorally characterized into an apperceptive and associative subtype according to their results on face memory and face perception tasks. Each DP subtype group was compared to an equal number of age- and sex-matched controls from the TD group. All participants were familiarized with one of two sets of face-identities via video. These identities were used as familiar face stimuli in the face-identity recognition task inside the scanner, with the untrained set serving as unfamiliar face stimuli. In the fMRI task, familiar or unfamiliar faces were presented in separate blocks (i.e., block design). In each block, participants determined if ‘test faces’ matched an initially presented ‘target face’. fMRI analyses focused on blood oxygenation level dependent (BOLD) responses during familiar and unfamiliar face-identity recognition within pre-defined regions of interest (ROIs): bilateral core-face network (OFA, pFFA, aFFA, aTL-FA) and extended network. Results: Behavioral deficits in 12 individuals were in accordance with an apperceptive DP subtype and 6 with an associative DP subtype. Behaviorally, in the face-identity recognition fMRI task, DPs performed significantly worse than matched controls during familiar (U = 12, p < 0.001) and unfamiliar (U = 12, p < 0.001) trials. On the neural level: the TD group recruited all pre-defined core-face regions during familiar and unfamiliar face-identity recognition. The OFA was more engaged during unfamiliar than familiar face-processing and responses in this region correlated with unfamiliar face-identity recognition performance. Unexpectedly, the aTL-FA was not more sensitive to familiar than unfamiliar faces. In DPs, distinct response profiles in apperceptive and associative subtypes were observed. Apperceptive DPs’ within-group analysis showed the aTL-FA is more sensitive to familiar than unfamiliar faces, while the OFA showed no increased sensitivity to unfamiliar faces. Compared to matched controls, they demonstrated overall reduced BOLD responses in specific core-face ROIs (i.e., bilateral OFA, pFFA, and aFFA) to unfamiliar faces (relative to familiar), most evident in the left OFA. In the same core-face ROIs increased responses to familiar than unfamiliar faces were detected. Responses in the bilateral OFA of apperceptive DPs positively correlated with unfamiliar face-identity recognition task performance. Associative DPs’ within-group analysis found no responses in the aTL-FA to either familiar or unfamiliar faces. Relative to matched controls, they had reduced responses in the right aFFA to both familiar and unfamiliar faces, as well as reduced left OFA responses to unfamiliar faces. In the extended network, both DP subtypes showed compensatory increased responses relative to their matched controls during familiar face-identity processing, with the apperceptive DP group exhibiting greater recruitment. Conclusion: In the TD brain, the present findings partially support a hierarchical model of face-identity processing: there was stronger recruitment of the bilateral OFA during unfamiliar face-identity recognition, underlining the increased perceptual processing necessary for recognizing unfamiliar faces. However, no elevated recruitment of anterior ROIs (i.e., aFFA, aTL-FA) during familiar face-identity recognition was found. In DPs, we find the characterization into subtypes is manifested in distinct neural response profiles. In apperceptive DPs, the behavioral face perception deficit may be attributed to reduced responses to unfamiliar faces in bilateral core-face ROIs (OFA, p/aFFA). The increased responses to familiar faces in core-face regions like the aTL-FA and extended network of this group may indicate compensatory recruitment or an interplay between the core-face and extended network. In associative DPs, we propose the exclusive face memory deficit may be reflected in reduced/missing responses in anterior core-face regions, i.e., aFFA and aTL-FA. Unexpectedly, the OFA of associative DPs does not respond like the TD group with higher sensitivity to unfamiliar faces. Associative DPs potentially recruit posterior core-face regions as compensation. Altogether, the findings emphasize the importance of bilateral posterior core-face regions for face perception, while challenging the notion of a strictly hierarchical face network. Based on these observations, we pose new questions regarding the organization of face-identity processing in TD and DP individuals and suggest a direct comparison of DP subtypes for future investigations.

Il existe de grandes variations interindividuelles dans les habiletés pour la reconnaissance des visages. Alors que plusieurs avenues ont été explorées pour expliquer ces variations, leur source reste inconnue. L’utilisation d’information visuelle étant reliée à la performance pour n’importe quelle tâche, l’objectif du projet était d’utiliser la méthode des Bulles pour évaluer comment l’information visuelle utilisée est liée aux habiletés. Ainsi, les habiletés pour la reconnaissance des visages ont été mesurées chez 107 participants, un large échantillon d’individus normaux provenant du spectre complet d’habiletés, incluant les extrêmes de ce spectre (i.e. prosopagnosie développementale et super-reconnaissance). Ensuite, une tâche de reconnaissance de visages célèbres a été complétée, utilisant la méthode des Bulles pour échantillonner aléatoirement l’information visuelle à chaque essai (1000). Une régression a permis de déterminer quelle information était échantillonnée de façon systématique lors des essais où le participant a répondu correctement. Cette opération résulte en une image de classification pour chaque participant, montrant l’information visuelle utilisée. Enfin, grâce à une régression de deuxième ordre, nous avons pu déterminer quelles sont les régions du visage dont l’utilisation permet de prédire les habiletés dans quatre tâches différentes. Les résultats montrent que 59% de la variation dans les habiletés peut être expliquée grâce à l’utilisation de certaines régions du visage. Plus spécifiquement, plus les participants font usage systématiquement de la région de l’œil gauche du point de vue de l'observateur, plus ils sont habiles. / Abilities for face recognition largely vary among neurotypical individuals. The source of these variations remains largely unknown. Because use of visual information affects performance for a task, the main objective of the project was to better understand the way in which visual information is used affects abilities for face recognition. To this end, we have used the Bubbles method to evaluate use of information in neurotypical participants from the complete spectrum of abilities for face recognition, including extreme cases (developmental prosopagnosics and super-recognizers). Therefore, face recognition abilities were measured in 107 participants prior to evaluating the visual information they use. In 1000 trials where participants were asked to identify a celebrity’s face, visual information was spatially randomly sampled using the Bubbles method. A regression was then applied between the location of the sampled information and accuracy on each trial, determining which information was systematically sampled when participants correctly identified faces. A second-order regression was then used, which determined the utilization of which regions of the face predicts ability scores, measured in four different tests. Results show that 59% of variations in abilities can be explained by the use of visual information for face recognition. Specifically, the more systematically participants use the region of the left eye, the more accurate they tend to be.

La capacité à reconnaître les visages de nos collègues, de nos amis et de nos proches est essentielle à notre réussite en tant qu'êtres sociaux. Notre cerveau accomplit cet exploit facilement et rapidement, dans une série d’opérations se déroulant en quelques dizaines de millisecondes à travers un vaste réseau cérébral du système visuel ventral. L’habileté à reconnaître les visages, par contre, varie considérablement d’une personne à l’autre. Certains individus, appelés «super-recognisers», sont capables de reconnaître des visages vus une seule fois dans la rue des années plus tôt. D’autres, appelés «prosopagnosiques», sont incapables de reconnaître le visage de leurs collègues ou leurs proches, même avec une vision parfaite. Une question simple reste encore largement sans réponse : quels mécanismes expliquent que certains individus sont meilleurs à reconnaître des visages? Cette thèse rapporte cinq articles étudiant les mécanismes perceptifs (articles 1, 2, 3) et cérébraux (articles 4, 5) derrière ces variations à travers différentes populations d’individus. L’article 1 décrit le contenu des représentations visuelles faciales chez une population avec un diagnostic de schizophrénie et d’anxiété sociale à l’aide d’une technique psychophysique Bubbles. Nous révélons pour la première fois les mécanismes en reconnaissance des expressions de cette population: un déficit de reconnaissance est accompagné par i) une sous-utilisation de la région des yeux des visages expressifs et ii) une sous-utilisation des détails fins. L’article 2 valide ensuite une nouvelle technique permettant de révéler simultanément le contenu visuel dans trois dimensions psychophysiques centrales pour le système visuel — la position, les fréquences spatiales, et l’orientation. L’article 3 a mesuré, à l'aide de cette nouvelle technique, le contenu représentationnel de 120 individus pendant la discrimination faciale du sexe et des expressions ( >500,000 observations). Nous avons observé de fortes corrélations entre l’habileté à discriminer le sexe et les expressions des visages, ainsi qu'entre l’habileté à discriminer le sexe et l’identité. Crucialement, plus un individu est habile en reconnaissance faciale, plus il utilise un contenu représentationnel similaire entre les tâches. L’article 4 a examiné les computations cérébrales de super-recognisers en utilisant l’électroencéphalographie haute-densité (EEG) et l’apprentissage automatique. Ces outils ont permis de décoder, pour la première fois, l’habileté en reconnaissance faciale à partir du cerveau avec jusqu’à 80% d’exactitude –– et ce à partir d’une seule seconde d’activité cérébrale. Nous avons ensuite utilisé la Representational Similarity Analysis (RSA) pour comparer les représentations cérébrales de nos participants à celles de modèles d’apprentissage profond visuels et langagiers. Les super-recognisers, comparé aux individus avec une habileté typique, ont des représentations cérébrales plus similaires aux computations visuelles et sémantiques de ces modèles optimaux. L’article 5 rapporte une investigation des computations cérébrales chez le cas le plus spécifique et documenté de prosopagnosie acquise, la patiente PS. Les mêmes outils computationnels et d’imagerie que ceux de l’article 4 ont permis i) de décoder les déficits d’identification faciale de PS à partir de son activité cérébrale EEG, et ii) de montrer pour la première fois que la prosopagnosie est associée à un déficit des computations visuelles de haut niveau et des computations cérébrales sémantiques. / The ability to recognise the faces of our colleagues, friends, and family members is critical to our success as social beings. Our brains accomplish this feat with astonishing ease and speed, in a series of operations taking place in tens of milliseconds across a vast brain network of the visual system. The ability to recognise faces, however, varies considerably from one person to another. Some individuals, called "super-recognisers", are able to recognise faces seen only once years earlier. Others, called "prosopagnosics", are unable to recognise the faces of their colleagues or relatives, even with perfect vision and typical intelligence. A simple question remains largely unanswered: what mechanisms explain why some individuals are better at recognizing faces? This thesis reports five articles studying the perceptual (article 1, 2, 3) and neural (article 4, 5) mechanisms behind these variations across different populations of individuals. Article 1 describes the content of visual representations of faces in a population with a comorbid diagnosis of schizophrenia and social anxiety disorder using an established psychophysical technique, Bubbles. We reveal for the first time the perceptual mechanisms of expression recognition in this population: a recognition deficit is accompanied by i) an underutilization of the eye region of expressive faces and ii) an underutilization of fine details. Article 2 then validates a new psychophysical technique that simultaneously reveals the visual content in three dimensions central to the visual system — position, spatial frequencies, and orientation. We do not know, however, whether skilled individuals perform well across a variety of facial recognition tasks and, if so, how they accomplish this feat. Article 3 measured, using the technique validated in article 2, the perceptual representations of 120 individuals during facial discrimination of gender and expressions (total of >500,000 trials). We observed strong correlations between the ability to discriminate gender and facial expressions, as well as between the ability to discriminate gender and identify faces. More importantly, we found a positive correlation between individual ability and the similarity of perceptual representations used across these tasks. Article 4 examined differences in brain dynamics between super-recognizers and typical individuals using high-density electroencephalography (EEG) and machine learning. These tools allowed us to decode, for the first time, facial recognition ability from the brain with up to 80% accuracy — using a mere second of brain activity. We then used Representational Similarity Analysis (RSA) to compare our participants' brain representations to those of deep learning models of object and language classification. This showed that super-recognisers, compared to individuals with typical perceptual abilites, had brain representations more similar to the visual and semantic computations of these optimal models. Article 5 reports an investigation of brain computations in the most specific and documented case of acquired prosopagnosia, patient PS. The same computational tools used in article 4 enabled us to decode PS's facial identification deficits from her brain dynamics. Crucially, associations between brain deep learning models showed for the first time that prosopagnosia is associated with deficits in high-level visual and semantic brain computations.

L’objectif de cette recherche est la création d’une plateforme en ligne qui permettrait d’examiner les différences individuelles de stratégies de traitement de l’information visuelle dans différentes tâches de catégorisation des visages. Le but d’une telle plateforme est de récolter des données de participants géographiquement dispersés et dont les habiletés en reconnaissance des visages sont variables. En effet, de nombreuses études ont montré qu’il existe de grande variabilité dans le spectre des habiletés à reconnaître les visages, allant de la prosopagnosie développementale (Susilo & Duchaine, 2013), un trouble de reconnaissance des visages en l’absence de lésion cérébrale, aux super-recognizers, des individus dont les habiletés en reconnaissance des visages sont au-dessus de la moyenne (Russell, Duchaine & Nakayama, 2009). Entre ces deux extrêmes, les habiletés en reconnaissance des visages dans la population normale varient. Afin de démontrer la faisabilité de la création d’une telle plateforme pour des individus d’habiletés très variables, nous avons adapté une tâche de reconnaissance de l’identité des visages de célébrités utilisant la méthode Bubbles (Gosselin & Schyns, 2001) et avons recruté 14 sujets contrôles et un sujet présentant une prosopagnosie développementale. Nous avons pu mettre en évidence l’importance des yeux et de la bouche dans l’identification des visages chez les sujets « normaux ». Les meilleurs participants semblent, au contraire, utiliser majoritairement le côté gauche du visage (l’œil gauche et le côté gauche de la bouche). / The present study aims to create a web-based platform that would examine individual differences in face processing strategies in different categorization tasks. The purpose of this platform is to collect data from geographically dispersed participants with variable face recognition abilities. Indeed, many studies have shown that there is high variability in the spectrum of face recognition ability, ranging from developmental prosopagnosia (Duchaine & Susilo, 2013), a disorder of face recognition in the absence of brain damage, to super-recognizers, individuals with extraordinary face recognition ability (Russell, Duchaine & Nakayama, 2009). Between these extremes, people vary substantially in their ability to recognize faces. To demonstrate the reliability of creating such a platform for individuals of widely varying abilities, we adapted a recognition task of the identity of famous faces using the Bubbles method (Gosselin & Schyns, 2001) and recruited 12 control subjects and a subject with developmental prosopagnosia. We were able to highlight the importance of the eyes and the mouth in face identification. The best observers seem mostly to use the left side of the face (left eye and the left side of the mouth).