پروزوپاگنوزیا اکتسابی اثر وارونگی صورت را الغا می کند

Abstract 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.

Introduction Individual faces are notoriously difficult to discriminate and recognize when they are presented upside-down (e.g., Hochberg and Galper, 1967 and Yin, 1969). This phenomenon has been known for decades and has generated tens or perhaps hundreds of studies in cognitive (neuro)science comparing behavioral performance and/or neural responses to upright and inverted face stimuli. While researchers still debate the cause(s) of this face inversion effect (FIE), most if not all authors in the field would acknowledge that inversion disrupts fundamental processes underlying our expertise at processing faces. Understanding the nature of the FIE is thus a major challenge for researchers in this field (Rossion, 2008). Another potential way to understand the nature of face processes through their disruption is by studying the behavior of brain-damaged patients who can no longer recognize individual faces, i.e., acquired prosopagnosia (AP). Prosopagnosia is classically defined as the inability to recognize individual faces following brain damage, an impairment which cannot be attributed to intellectual deficiencies or low-level visual problems (Quaglino and Borelli, 1867, Bodamer, 1947 and Rondot and Tzavaras, 1969). The nature of the face processing impairment in prosopagnosia has also been debated in the literature for decades (e.g., Rondot and Tzavaras, 1969, Damasio et al., 1982 and Sergent and Signoret, 1992). While some authors have emphasized the variety of functional deficits among patients (Sergent and Signoret, 1992 and Schweich and Bruyer, 1993), there are striking similarities among many cases of prosopagnosia, even when the localization of their brain lesions differs greatly. In many reports, AP has been associated with a deficit in holistic/configural face processing, i.e., a defect at integrating simultaneously the multiple features of a face into a single global perceptual representation (e.g., Galli, 1964, Levine and Calvanio, 1989, Sergent and Villemure, 1989, Sergent and Signoret, 1992, Saumier et al., 2001 and Boutsen and Humphreys, 2002). More recently, it has also been found that prosopagnosic patients have particular difficulties at extracting diagnostic information from the eyes (Caldara et al., 2005 and Bukach et al., 2006), a region of the face that is made of multiple elements, or at perceiving relative distances between features (Barton et al., 2002). These two aspects of prosopagnosia may also be related to a loss of holistic face processing (Rossion, 2008). How do AP patients process upright and inverted faces? In principle, clarifying this relationship between prosopagnosia and inversion is potentially important because it could shed light on both the nature of face inversion and prosopagnosia, in particular reinforcing or questioning the view that the (in)ability to process individual faces holistically is at the heart of the AP syndrome. If the outcome of brain damage on putative expert face processes is as detrimental as inverting the face stimulus for normal observers, so to speak, one would expect that AP patients do not show a normal FIE: it should be seriously reduced or even abolished. However, even when considering only the experiments performed with whole upright and inverted faces in individual discrimination/recognition tasks, four different outcomes have been observed: (1) an absence of inversion cost in several cases ( McNeil and Warrington, 1991, case 2 in accuracy and RTs; Boutsen and Humphreys, 2002, patient HJA in accuracy; Delvenne et al., 2004, patient NS in accuracy and RTs); (2) a reduced FIE in two cases tested with manipulations of local and relational cues for individualizing faces ( Barton et al., 2003, patient TS in accuracy; Bukach et al., 2006, patient LR in accuracy); (3) a normal effect in one patient ( Anaki et al., 2007, patient DBO in accuracy and RTs); and (4) a reverted inversion effect, namely a better performance for inverted faces in some cases ( Farah et al., 1995a, Farah et al., 1995b and de Gelder and Rouw, 2000a, 2000b, patient LH in accuracy and RTs; de Gelder et al., 1998, patient AD in accuracy). In addition, there are ambiguous cases (e.g., Riddoch et al., 2008, patient FB, reverted trend in RTs for same responses, but normal effect with different responses) and inconsistencies in the results reported for the same patients in the literature. For example, the (prosop)agnosic patients CR, SM and RN were tested in several studies ( Gauthier et al., 1999, Marotta et al., 2002 and Behrmann et al., 2005). Gauthier et al. (1999) reported large inversion effects in both accuracy and RTs for CR and SM. In another study ( Marotta et al., 2002), CR still performed better with upright faces, but was significantly faster for inverted faces, contrary to controls, suggesting a speed-accuracy trade-off. In that study, the patient RN did not show any effect in accuracy but a normal inversion effect in RTs ( Marotta et al., 2002). However, most recently, all three patients, considered as a group, were reported as performing slightly better and faster with inverted faces ( Behrmann et al., 2005). Thus, overall, the outcome of inversion on individual face processing in AP remains unclear. One way to account for the variability across patients is by acknowledging the great variability in terms of functional impairments of AP, following different lesion localization(s) and aetiologies, as well as putative compensatory strategies (Sergent and Signoret, 1992 and Schweich and Bruyer, 1993). However, when considering the literature on face inversion and prosopagnosia attentively, one cannot help noting a number of methodological issues in patient selection, tasks performed, variables measured and analyzed, as well as possible overinterpretations of some observations. As a result, the variety of outcomes reported about inversion effects in prosopagnosia may equally well have been created by the different kinds of experiments performed rather than reflecting a true functional variability in terms of face processes. This argument is supported by several observations. First, as noted above, there are inconsistencies in the results reported for the same patients in the literature (e.g., Gauthier et al., 1999, Marotta et al., 2002 and Behrmann et al., 2005). These opposite patterns across studies, observed during individual face matching tasks in the same brain-damaged patients, cast doubts on the conclusions that can be drawn from these studies at least regarding the FIE in prosopagnosia. It is worth noting also that these cases were close to chance level with upright faces in several experiments, making difficult to draw clear conclusions. Second, many studies do not measure or report correct RTs during individual face processing tasks (e.g., de Gelder et al., 1998, de Gelder and Rouw, 2000a, de Gelder and Rouw, 2000b and Boutsen and Humphreys, 2002). Yet, it is known that when having to match/discriminate individual faces, prosopagnosic patients can achieve reasonably high scores by using unnatural (i.e., analytical) strategies ( Davidoff and Landis, 1990 and Farah, 1990), which may be revealed by abnormally long RTs. Moreover, correct RTs are a highly sensitive measure of the effects of face inversion in normal observers (see Rossion, 2008). Most importantly, when RTs are measured in studies of face inversion in prosopagnosia, they are rarely considered with respect to accuracy to rule out potential speed-accuracy trade-offs effects (e.g., Marotta et al., 2002), or combined with accuracy to obtain a global face inversion index. Third, most studies do not compare the processing of upright and inverted faces to non-face objects presented at the two orientations ( McNeil and Warrington, 1991, Farah et al., 1995a, Farah et al., 1995b, Marotta et al., 2002, Delvenne et al., 2004, Behrmann et al., 2005 and Anaki et al., 2007). However, it may be important to monitor for general effects of picture inversion, which may not be directly related to the ability to process faces. For instance, LH, the only patient who clearly presents a better performance for inverted than upright faces both in accuracy and RTs ( Farah et al., 1995a and Farah et al., 1995b), shows the exact same pattern for pictures of non-face objects (shoes; de Gelder and Rouw, 2000a). Strangely enough, these non-face objects do not even lead to inversion costs for normal observers ( de Gelder et al., 1998). This suggests that LH's relative inversion superiority in processing inverted items may be due to a general visual impairment rather than face processes per se (e.g., his massive upper visual field defects, see Levine and Calvanio, 1989). Fourth, tasks and stimuli used differ greatly across studies: same/different (AX) discrimination or 2-alternative forced choice paradigms (ABX), with simultaneous presentations of all items or delayed presentations (AX; ABX), etc. During same/different (AX) discrimination tasks, response biases can arise (e.g., the patient responding systematically that the faces are identical), making impossible to interpret the results on “different” trials (e.g., Gauthier et al., 1999 and Boutsen and Humphreys, 2002). Moreover, large variations in presentations times have been used during delayed matching tasks [from 400 msec ( Anaki et al., 2007) to 10 sec ( Farah et al., 1995a and Farah et al., 1995b)]. Fifth, another major factor limiting the interpretation of the outcome of previous experiments is that all the patients tested with upright and inverted faces so far present clear general visual recognition problems, in particular with objects (excepted FB, Riddoch et al., 2008) besides their face recognition impairments, preventing to assess clearly the relative inversion costs for faces and nonface objects. Finally, as noted above, these patients present important low-level visual defects ( McNeil and Warrington, 1991, Farah et al., 1995a, Farah et al., 1995b, Boutsen and Humphreys, 2002, Delvenne et al., 2004 and Anaki et al., 2007), as often found in cases of prosopagnosia following brain damage. Given all these reasons, we aimed at reinvestigating the question of how AP patients process upright and inverted faces, in order to shed light on both the nature of the FIE and AP. We took advantage of the opportunity to test extensively a well-described case of AP with no object recognition impairment, and largely preserved low-level visual abilities (PS, Rossion et al., 2003). The patient was tested in 5 different behavioral experiments with upright and inverted faces and her results were contrasted with a carefully selected population of age-matched controls for each experiment. We used different stimuli and paradigms, avoided response biases (2-alternative forced choice matching tasks), measured both accuracy rates and correct response times to assess speed-accuracy trade-offs and display global indexes of inversion costs, and compared the effect of inversion to another category of mono-oriented stimuli (Experiments 3 and 4). Finally, given that the patient is in daily contact with a large set of homogenous faces (children of a kindergarten), we also had the opportunity to assess for the first time the FIE in prosopagnosia during familiar face recognition. Over all experiments, the results were highly consistent, showing an absence of face inversion cost for the prosopagnosic patient PS. There was no hint of inversion superiority. We discuss these observations in the context of previous case studies and the nature of the FIE, arguing that a significant reduction of the FIE in prosopagnosia is not only the most observable pattern following a careful look at the literature, but it is also the most plausible, from a theoretical point of view.

5. Conclusions Here we report an extensive and complete investigation of upright and inverted individual face processing in a case of selective AP. The results indicate an absence of inversion effect in this patient. An overview of the literature supports the view that acquired prosopagnosic patients present an abolished or reduced inversion effect, rather than a rare pattern of inversion superiority that is likely due to low-level visual defects. Our findings reinforce the view that a key aspect of the impairment in AP lies in the inability to form a holistic representation of the individual face.