Brief CommunicationImpairment of holistic face perception following right occipito-temporal damage in prosopagnosia: Converging evidence from gaze-contingency
Introduction
The scientific literature about the mechanisms responsible for the remarkable ability with which humans can recognize faces has traditionally been characterized by a debate about the relative contribution of an analytical vs. holistic way of processing the visual stimulus. Analytical processing involves selecting first the most diagnostic information from the face in a local part-by-part fashion, bringing the information from different parts together only at a later stage. Evidence for this processing mode in face recognition tasks comes from studies showing that it is indeed possible to recognize faces based on parts only (e.g., Davies et al., 1977, Sadr et al., 2003) and that facial parts such as the eyes seem to be more important for face recognition than others, as shown by eye tracking studies (e.g., Yarbus, 1967) and response classification experiments (e.g., Gosselin and Schyns, 2001, Haig, 1985). However, other studies show that facial parts are processed interactively, whereby perception of one part is influenced by how we perceive the other parts, as demonstrated by the whole-part face superiority effect (Tanaka & Farah, 1993) and the composite face effect (Young, Hellawell, & Hay, 1987). Along these lines, proponents of the holistic processing view claim that faces are first perceived as a whole rather than a collection of independent parts (Galton, 1883), perhaps as a coarse global representation that can be gradually refined over time (Sergent, 1984, Watt, 1987).
Gaze-contingency is a method that was originally used to investigate the perceptual span in reading (Rayner, 1975) and later in visual scene recognition (van Diepen, Wampers, d’Ydewalle, & Underwood, 1998). Recently, introducing this method in face perception research allowed investigating the amount and type of information that could be simultaneously perceived and potentially used during a face perception task (Van Belle et al., 2010a, Van Belle et al., 2010b). More specifically, Van Belle, De Graef, Verfaillie, Busigny, et al. (2010a) used gaze-contingency to test a well-known brain-damaged patient presenting with a face-specific recognition impairment (prosopagnosia, Bodamer, 1947). In a delayed face matching task, the prosopagnosic patient PS (Rossion et al., 2003) was relatively less impaired than typical observers if she was forced to analyze the faces part-by-part through a gaze-contingent window. In contrast, if a gaze-contingent mask obstructed only her fixated part, the patient's performance decreased dramatically as compared to normal observers.
These results led to the conclusion that the cause of PS’ face recognition impairment is the inability to perceive individual faces holistically, supporting the view that holistic perception is necessary for visual expertise in processing faces.
So far, these findings were obtained in only one case of prosopagnosia, a patient who has distributed lesions, including a large lesion in the right inferior occipital cortex, in the left middle fusiform gyrus, and to a smaller extent in the right middle temporal gyrus (Sorger, Goebel, Schiltz, & Rossion, 2007). Nevertheless, there is evidence that holistic perception of individual faces is primarily a function of the right hemisphere (e.g., Hillger and Koenig, 1991, Schiltz and Rossion, 2006), and it has been suggested that an impairment of this function is a common characteristic of all cases of prosopagnosia following brain damage (Ramon, Busigny & Rossion, 2010; see also Barton, Press, Keenan, & Connor, 2002). To provide further evidence for these views, and more generally help getting a clearer view on the neural mechanisms responsible for holistic processing, the present study reports the test of the same gaze-contingency experiment on another case of acquired prosopagnosia (GG, Busigny et al., 2010). Contrary to PS, GG has a single lesion, unilaterally in the right hemisphere, which encompasses a large section of the medial section of the ventral occipito-temporal cortex including the lingual, medial fusiform, and parahippocampal gyri. Despite the extent of the brain damage, his object recognition is entirely preserved, so that, like PS, GG suffers from a face-specific visual agnosia (“pure prosopagnosia”, see Busigny et al., 2010).
Section snippets
Materials and methods
GG is a right-handed male born in 1942 who suffered from brain damage after a cerebral vascular accident in 2002. His remaining complaints are a left hemianopia and prosopagnosia. GG's object recognition and perception is intact, even for tasks requiring holistic processing of objects (for more details about GG's case, see Busigny et al., 2010).
The course of a trial in the delayed face matching task was identical to the study with PS (see Fig. 2 in Van Belle et al., 2010a). Each trial started
Behavioral data
For normal observers, performance differed significantly between conditions (main effects: accuracy rates: F(2, 12) = 8.45; p = .005, RT: F(2, 12) = 11.53; p = .0016, number of fixations: F(2, 12) = 16.97; p = .0003). Specifically, performance was higher in full view than with the mask (Accuracy: t(12) = 3.88; p = .006, RT: t(12) = 4.78; p = .0012, fixations: t(12) = 5.78; p = .0002), and the window (t(12) = 3.13; p = .022, t(12) = 2.77; p = .042, t(12) = 2.28; p = .098, respectively). Accuracy and response times in the mask and
Discussion
Like the previously reported case of acquired prosopagnosia PS, GG has a strong impairment with the central mask condition when matching/discriminating individual faces. This condition prevents using the fixated part, and thus promotes reliance on holistic perception to realize the task. In contrast, GG showed a similar performance level as controls in the window condition, the condition that forces relying on a single part at a time. This observation demonstrates again the key role of holistic
Acknowledgements
We thank all participants for their cooperation. GVB, TB and BR are supported by the Belgian National Fund for Scientific Research (FNRS). This work was supported by grants from the PRODEX program, FNRS (MIS), Action de Recherche Concertée (Belgium), and the European Space Agency of the European Union. This paper presents research results of the Belgian Network DYSCO (Dynamical Systems, Control and Optimization), funded by the Interuniversity Attraction Poles Programmes, initiated by the
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