پردازش جامع اختلال در چهره فردی ناآشنا در پروزوپاگنوزیای اکتسابی

Abstract 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 patient's 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

. Introduction Brain damage to bilateral or right unilateral occipito-temporal regions can cause a massive impairment at recognizing familiar faces. This rare neurological condition has been termed ‘prosopagnosia’ (Bodamer, 1947) and has attained a considerable degree of popularity in the neuropsychological literature since the first clinical observations (Quaglino et al., 2003 and Wigan, 1844). The clinical and anatomical conditions of prosopagnosia have been of great interest to cognitive neuroscientists willing to clarify the neuro-functional mechanisms of normal face processing. For instance, the study of prosopagnosia is at the origin of the idea that there are neural processes devoted exclusively to faces in the adult human brain (Bodamer, 1947). Anatomical descriptions of prosopagnosia have also provided the first and strongest evidence for the critical role of the right occipito-temporal cortex in face recognition (Meadows, 1974, Landis et al., 1988, Michel et al., 1989, Sergent and Signoret, 1992a, Barton et al., 2002 and Bouvier and Engel, 2006). However, despite the relatively large number of cases of acquired prosopagnosia (AP) reported since the first descriptions, there is yet no unified account for these patients’ inability to recognize or discriminate individuals by means of their faces. Following early proposals (e.g., Levine and Calvanio, 1989 and Sergent and Villemure, 1989), it has been suggested that AP patients suffer from an inability to process faces configurally/holistically.1Levine and Calvanio (1989) described the patient LH as being unable to “get an immediate overview of a face […] as a whole at a single glance” (p.159). Following experiments with non-face patterns and tests of visual closure, these authors concluded that AP represents a general loss of visual “configural [i.e. holistic] processing”—a view supported by subsequent observations. A number of studies have inferred a deficit of holistic face processing (HP) in prosopagnosia from an abnormal effect of face inversion: contrary to controls the patients either showed a reduced effect, or no performance decrease at all (e.g., Gauthier et al., 1999, Marotta et al., 2002 and Delvenne et al., 2004), or even a paradoxical superior performance with inverted faces (e.g., Farah, Wilson, Drain, & Tanaka, 1995; but see Busigny & Rossion, 2009). However, since the nature of the face inversion effect remains a matter of debate (Rossion, 2008a), abnormal effects of inversion in AP provide only indirect evidence that the cause of the processing impairment is a deficit of HP (see Busigny & Rossion, 2009, for a recent discussion). Other authors have followed Levine and Calvanio's (1989) approach and showed general holistic processing impairments in AP with non-face stimuli (overlapping figures, Gestalt-completion figures, global texture, dot patterns, hierarchical Navon stimuli, … e.g., Evans et al., 1995 and Takahashi et al., 1995; for a review of global/holistic processing in object perception in general see also Kimchi, 1992). A lack of HP in prosopagnosia has been more directly and specifically inferred from observations made based on matching or priming experiments with schematic faces made of multiple features, and multidimensional analysis (Sergent and Villemure, 1989, Sergent and Signoret, 1992b and Saumier et al., 2001), or from whole–part interference paradigms such as the Thatcher illusion (Boutsen and Humphreys, 2002 and Riddoch et al., 2008). Finally, some authors have emphasized the difficulty of AP patients in processing relative distances between features (Barton et al., 2002 and Joubert et al., 2003), a type of information diagnostic for face individuation that has been characterized as “configural” (Carey, 1992 and Maurer et al., 2002). Together, these studies have provided some evidence supporting the view that AP is characterized by a particular lack of the ability to integrate facial features into a global (i.e., holistic) representation. However, more compelling evidence to support the above-mentioned hypothesis may be necessary, for at least two reasons. First, all studies (with the exception of one case in Sergent & Signoret, 1992a, and one recent case by Riddoch et al., 2008) have tested patients presenting clear basic-level object recognition impairments (Levine and Calvanio, 1989 and Sergent and Signoret, 1992a, two cases; Farah et al., 1995, Evans et al., 1995, Takahashi et al., 1995, de Gelder et al., 1998, Gauthier et al., 1999, Saumier et al., 2001, Barton et al., 2002, Boutsen and Humphreys, 2002, Marotta et al., 2002, Delvenne et al., 2004 and Anaki et al., 2007). Thus, while Levine and Calvanio's (1989) view is that AP represents a general loss of visual “configural [i.e. holistic] processing”, this hypothesis may require further investigation from single case studies of patients presenting a selective deficit for face recognition, tested for their holistic processing abilities with face (rather then object) stimuli. Second, there are two paradigms that have been used extensively in the behavioral literature with normal viewers to demonstrate HP: the composite face paradigm (Young, Hellawell, & Hay, 1987) and the whole-part paradigm (Tanaka & Farah, 1993). Both reveal effects that are acknowledged to demonstrate holistic processing of facial features (Maurer et al., 2002, McKone and Robbins, 2007 and Rossion, 2008a). While variants of the whole/part paradigm have been tested with visual agnosic patients (e.g., Boutsen & Humphreys, 2002), the composite face paradigm, which is more consistently used and gives more robust holistic effects has not been tested in AP (see Le Grand, Mondloch, Maurer, & Brent, 2003, for composite face effects tested in congenital prosopagnosia). Since these effects have been well demonstrated in the normal population, and are acknowledged to be highly sensitive at measuring HP, an absence or reduction of composite and whole/part effects in a case of AP would provide strong evidence for HP difficulties. Taking into account these issues, we tested HP of the prosopagnosic patient PS, who suffers from a selective deficit at recognizing and matching individual faces following brain damage (Rossion et al., 2003), applying both the whole/part and composite face paradigms, across five experiments. In line with previous proposals (e.g., Galton, 1883, Goldstein and Chance, 1980, Farah et al., 1998 and Ingvalson and Wenger, 2005), here we conceptualize HP as the “simultaneous perception of the multiple features of an individual face, that are integrated into a single global representation” ( Rossion, 2008a). A direct consequence of this holistic mode of processing is that normally a given facial feature cannot be processed independently of the other features. We hypothesize that the patient PS – deprived of this holistic mode of processing faces – would process a given facial feature without being influenced by other features of the whole face.