Detailed Exploration of Face-Related Processing in Congenital Prosopagnosia: 1
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Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 1. Behavioral Findings Marlene Behrmann1, Galia Avidan1, Jonathan J. Marotta2, and Rutie Kimchi3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/7/1130/1757302/0898929054475154.pdf by guest on 18 May 2021 Abstract & We show that five individuals with congenital prosopagnosia to a more fundamental visual processing disorder; the CP in- (CP) are impaired at face recognition and discrimination and dividuals exhibited difficulty in deriving global configurations do not exhibit the normal superiority for upright over in- from simple visual stimuli, even with extended exposure dura- verted faces despite intact visual acuity, low-level vision and tion and considerable perceptual support in the image. De- intelligence, and in the absence of any obvious neural riving a global configuration from local components is more concomitant. Interestingly, the deficit is not limited to faces: critical for faces than for other objects, perhaps accounting The CP individuals were also impaired at discriminating com- for the exaggerated deficit in face processing. These findings mon objects and novel objects although to a lesser extent than elucidate the psychological mechanisms underlying CP and discriminating faces. The perceptual deficit may be attributable support the link between configural and face processing. & INTRODUCTION Avidan, 2005; Duchaine & Nakayama, 2005; Kress & Congenital prosopagnosia (CP) refers to the lifelong Daum, 2003a). However, many findings remain incon- impairment in face processing that is apparent from sistent, perhaps as a function of the paucity of cases, the birth, despite intact visual and intellectual functions. apparent heterogeneity of the disorder and/or the vary- The term ‘‘congenital’’ is used to denote the absence ing methods of assessment. of a lesion or other neurological concomitant acquired Although an impairment in face processing is de facto at any stage of development (Jones & Tranel, 2001), and required for the diagnosis of CP, face processing is not excludes individuals suffering from visual deprivation, monolithic and can involve detecting the presence of a as in cases of infantile cataracts, or from other de- face, discriminating between two faces or identifying an velopmental problems such as autism. CP also contrasts individual face. Which of these processes is implicated in with the more general term ‘‘developmental prosopag- CP is unclear; although some CP individuals succeed in nosia,’’ which includes CP as well as individuals who relatively easy matching tasks (perhaps by matching in- have sustained brain damage before birth or in early dividual features), when reaction time (RT) is measured childhood (Barton, Cherkasova, Press, Intriligator, & and task demands are increased, the deficit is uncovered O’Connor, 2003; Farah, Rabinowitz, Quinn, & Liu, 2000). (Kress & Daum, 2003a). The extent to which CP indi- CP can be severely debilitating, affecting the recognition viduals can recognize famous faces has also yielded of even the most familiar individuals (Nunn, Postma, & mixed results: some perform poorly (de Gelder & Rouw, Pearson, 2001). These CP individuals may also fail to 2000; Bentin, Deouell, & Soroker, 1999), whereas others discriminate between two unknown faces, usually rec- perform quite well (Duchaine & Nakayama, 2005; Duch- ognizing others by voice or other cues such as clothing aine, 2000; Temple, 1992). Note that the images used in or accessories. As in acquired prosopagnosia (AP), CP these tests often contain salient cues such as clothing; individuals are typically able to acknowledge that a face because CP individuals are particularly adept at exploit- is present but are unable to assign identity to the face. ing such cues, these latter cases may compensate for Unlike AP, however, CP may go undetected as the in- the underlying recognition deficit. The heterogeneity of dividual has no means of comparison with normal findings clearly calls for a systematic analysis of face face processing skills. In the last couple of years, there processing in CP. has been increasing interest in CP (e.g., Behrmann & A second relevant issue, which remains the subject of an ongoing controversy, is the extent to which prosopagnosia (AP and CP) is specific to faces. Neuro- 1Carnegie Mellon University, Pittsburgh, 2University of Mani- psychological studies have demonstrated a double dis- toba, Winnipeg, 3University of Haifa sociation between the recognition of faces and objects D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:7, pp. 1130–1149 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929054475154 by guest on 01 October 2021 (Moscovitch, Winocur, & Behrmann, 1997; McNeil & 1988). The failure to integrate visual elements is thought Warrington, 1993), and functional imaging (Kanwisher, to underlie prosopagnosia (Barton, Press, Keenan, & McDermott, & Chun, 1997), ERP (Bentin, Allison, Puce, O’Connor, 2002; Levine & Calvanio, 1989), with the Perez, & McCarthy, 1996), and physiology (Rolls, 1984; result that these patients rely on a more piecemeal or Perrett, Rolls, & Caan, 1979) studies point to the exis- feature-based strategy in constructing face representa- tence of a neural system specialized, if not dedicated, to tions. Although the failure to derive configurations is faces (Behrmann & Moscovitch, 2001). An alternative thought to be particularly devastating for face process- view, which also has widespread support, is that there is ing, given the homogeneity between exemplars and the a general-purpose visual process that subserves all visual need to rely on the second-order statistics of the input objects and the dissociations arise because of the un- (Rhodes, 1988), a configural impairment may affect Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/7/1130/1757302/0898929054475154.pdf by guest on 18 May 2021 usual demands placed on the system by faces (Tarr & other nonface stimuli, too, if the spatial relations be- Cheng, 2003). Because face processing typically involves tween the components are required to differentiate per- individual identification, whereas other objects are usu- ceptually similar exemplars. ally recognized at a basic level (e.g., as a chair or an The purpose of the current article is to explore these apple), faces engage fine-grained discrimination of per- three issues in a group of five adults with CP. Our ceptually similar exemplars within a category and indi- findings show that all CP subjects are impaired at face viduals become expert at these discriminations. Whether recognition and discrimination, and do not show the recognition of other visual nonface objects is also im- well-known benefit for upright over inverted faces. paired when homogeneous, complex stimuli are em- Interestingly, all of these same individuals are impaired ployed remains debatable. Many AP individuals have at nonface object recognition, although this is much difficulties categorizing exemplars of within-class ob- more variable and less severe than their face processing jects, which share the same complex configuration difficulty. Finally, all subjects are impaired at configural (Gauthier, Behrmann, & Tarr, 1999; De Haan and Camp- processing, exhibiting difficulty in deriving the global bell, 1991; Etcoff, Freeman, & Cave, 1991; Damasio, configuration of even very simple visual images, letters, Damasio, & Hoesen, 1982), although this does not seem and geometric shapes. The apparent failure to extract to be true for all cases (Farah, Wilson, Drain, & Tanaka, the spatial relations between the local elements is 1995; Sergent & Signoret, 1992; De Renzi, Faglioni, conjectured to contribute to the disproportionate failure Grossi, & Nichelli, 1991). to process faces, relative to other visual stimuli. In a review of nine cases of CP, two are impaired at recognizing nonface objects, one mildly and one severe- ly (Kress & Daum, 2003a) and, in a recent study, using RESULTS an old/new recognition memory paradigm, four out of A group of five CP individuals participated in three series seven CP individuals showed a dissociation between of studies, each addressing one of the issues laid out memory for faces and objects (Duchaine & Nakayama, above. In all five individuals, CP was manifested without 2005). We note, however, that the methods of as- any obvious underlying neurological cause, and visual sessment vary considerably across studies and that acuity and basic visual processing abilities were unim- reaction time is generally not measured despite the paired (see Table 1 for biographical details and results possibility that the CP individuals might be inordinately of low-level visual tasks). We compared the performance slow or might even trade speed off against accuracy. To explore the specificity of the deficit, then, we ex- amine the performance of the CP individuals in tasks Table 1. Congenital Prosopagnosic Subjects using common objects and novel objects under condi- tions where the task demands and measurements are CP Subjects’ Log Contrast Gabor Contour Initials Sex Age Thresholdsa Detection Áb equated, as closely as possible, to those required for face discrimination. TM M 27 normal .65 The final major issue concerns the relationship be- KM F 60 normal .7 tween face processing and configural perception. Faces form a class of perceptually similar visual stimuli and are, NI M 40 normal .55 therefore, thought to be the paradigmatic example