Perceptual expertise effects are ...
Perceptual Expertise Effects Are Not All or None: Spatially Limited Perceptual Expertise for Faces in a Case of Prosopagnosia Cindy M. Bukach1, Daniel N. Bub2, Isabel Gauthier1, and Michael J. Tarr3 Abstract & We document a seemingly unique case of severe proso- pagnosia, L. R., who suffered damage to his anterior and inferior right temporal lobe as a result of a motor vehicle accident. We systematically investigated each of three factors associated with expert face recognition: fine-level discrimina- tion, holistic processing, and configural processing (Experi- ments 1���3). Surprisingly, L. R. shows preservation of all three of these processes that is, his performance in these experi- ments is comparable to that of normal controls. However, L. R. is only able to apply these processes over a limited spatial extent to the fine-level detail within faces. Thus, when the location of a given change is unpredictable (Experiment 3), L. R. exhibits normal detection of features and spatial configurations only for the lower half of each face. Similarly, when required to divide his attention over multiple face features, L. R. is able to determine the identity of only a single feature (Experiment 4). We discuss these results in the context of forming a better understanding of prosopagnosia and the mechanisms used in face recognition and visual expertise. We conclude that these mechanisms are not ������all-or-none,������ but rather can be impaired incrementally, such that they may remain functional over a restricted spatial area. This conclusion is consistent with previous research suggesting that perceptual expertise is acquired in a spatially incremental manner [Gauthier, I., & Tarr, M. J. Unraveling mechanisms for expert object recog- nition: Bridging brain activity and behavior. Journal of Experimental Psychology: Human Perception & Performance, 28, 431���446, 2002]. & INTRODUCTION Prosopagnosia (a face recognition deficit) can be con- ceptualized as a loss of, or reduced access to, previously acquired perceptual expertise with faces (Gauthier, Behrmann, & Tarr, 1999). Studies of prosopagnosia tend to isolate the deficit to a particular process such as configural processing (e.g., Barton, Press, Keenan, & O���Conner, 2002 Levine & Calvanio, 1989). However, it may be that perceptual mechanisms are not necessarily lost in an ������all-or-none������ fashion. Expertise-training stud- ies with novel objects (Greebles) suggest that expertise is acquired incrementally over an expanding spatial window (Gauthier & Tarr, 2002), and thus, its loss may also follow a similar spatial gradient. We present a study of a prosopagnosic case, L. R., which suggests that expertise effects are not all-or-none, but may be lost incrementally, such that they remain functional over a spatially restricted area. A General Framework for Studying Face Recognition Deficits Research on impaired face processing in brain-injured individuals has been motivated by two alternative views of the relation between the mechanisms responsible for face recognition and those mediating the recogni- tion of other object categories. One view is that such impairments result from the loss of distinct mecha- nisms that are domain specific to faces. This ������domain- specific������ interpretation of prosopagnosia is based on evidence from tasks that contrast impaired perform- ance for face stimuli with intact performance for nonface stimuli (e.g., Nunn, Postma, & Pearson, 2001 Henke, Schweinberger, Grigo, Klos, & Sommer, 1998 Farah, Levinson, & Klein, 1995 McNeil & Warrington, 1991). However, such comparisons may not always be equated for factors such as level of difficulty, response times, response bias, or level of expertise (Gauthier, Behrmann, & Tarr, 1999 Sergent & Signoret 1992b). Thus far, only a single case has been documented that shows the reverse pattern (intact performance on faces but impaired recognition of objects Moscovitch, Winocur, & Behrmann, 1997). 1Vanderbilt University, 2University of Victoria, 3Brown University D 2006 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 18:1, pp. 48���63
The alternative view is that prosopagnosia results from the loss of one or more perceptual processes that underlie expertise with objects that are identified at an individual level and that are members of homog- eneous categories. This ������perceptual-expertise������ inter- pretation of prosopagnosia is based on evidence that shows a functional association between face recogni- tion deficits and abnormal performance for objects (Gauthier, Behrmann, & Tarr, 1999). The rationale is that once the impaired process in a case of prosopagnosia is identified, a deficit should be evident for both faces and objects, providing the task requires the impaired process for both faces and objects. Although association method- ology has been criticized because co-occurring deficits may simply reflect anatomically proximal but indepen- dent mechanisms (for a discussion, see Shallice, 1988), this weakness can be overcome by an a priori theoretical framework built on evidence from the study of normal face perception. Although we realize that the issue of domain spec- ificity in prosopagnosia continues to be debated (e.g., Duchaine, Dingle, Butterworth, & Nakayama, 2004 Gauthier, Behrmann, & Tarr, 2004), here we address a different question: Can prosopagnosic patients dem- onstrate evidence for partial preservation of face ex- pertise that resembles the performance of trainees at intermediate levels of expertise? Although a spatial gradient of impairment is orthogonal to the domain- specific debate, currently, the expertise framework is the only account that can explain or predict such a pattern of loss. Thus, to answer this question, we apply an expertise framework to the study of a prosopagno- sic patient, L. R., and systematically test the processes that are known to be important to the development and utilization of perceptual expertise. This methodol- ogy has two important benefits: First, it allows us to rule out many potential hypotheses regarding the cause of L. R.���s deficit with faces and to place his deficit in the context of a well-specified theoretical framework. This is particularly useful because proso- pagnosia, like many neurological syndromes, is not a unitary phenomenon rather, many kinds of impair- ments can lead to selective difficulty in the perception or identification of faces. Second, the application of a general framework of generic object recognition to investigations of prosopagnosia allows for stronger generalizations from single-case studies to normal ob- ject recognition processes. An expertise framework is especially useful for two reasons: First, the spatial restric- tion on L. R.���s expert face processing generalizes to nonface objects such as Greebles (Bukach, Bub, Kadlec, Gauthier, & Tarr, in preparation). Second, the spatial restrictions on L. R.���s fine-level processing can best be explained within the expertise framework and related experiments that have found that the acquisition of expertise mechanisms also occurs in a spatially graded manner (Gauthier & Tarr, 2002). Several factors have been proposed to distinguish expert face recognition mechanisms from the mecha- nisms that are used to identify other object classes. First, faces more than other objects require the ability to make fine-level discriminations (Damasio, 1990 Damasio, Damasio, & Van Hoesen, 1982). This inequality is the result of differences in both task demands and stimulus characteristics. Face recognition is more demanding of discrimination processes because it involves identifica- tion at an individual or subordinate level, whereas most other object recognition requires only basic-level iden- tification (Rosch, Mervis, Gray, Johnson, & Boyes-Braem, 1976). Discrimination skills are also more taxed by faces because of the homogeneity of faces as a stimulus class. For instance, Gauthier, Behrmann, and Tarr (1999) suggested that a general deficit in fine-level discrimina- tion would interfere with subordinate-level judgments not only for faces, but also for any homogeneous object class, providing the task was sufficiently difficult (from the standpoint of high visual similarity between objects that must be discriminated from one another). To test this hypothesis, they manipulated level of categorization within several object categories and compared the per- formance of two prosopagnosic subjects to normal controls. When judgments required subtle discrimina- tions at more subordinate levels, the performance of the prosopagnosic subjects was dramatically impaired, re- gardless of stimulus class (see also Viele, Kass, Tarr, Behrmann, & Gauthier, 2002). A second distinction that has been made between face and object recognition is the degree to which faces are processed holistically (Levine & Calvanio, 1989 Davidoff, Matthews, & Newcombe, 1986). Evidence for holistic processing of faces is based in part on the finding that details of one part of a face influence the perception of another part of the face. For example, a change to the shape of the eyes impairs recognition of the unaltered mouth (Farah, Wilson, Drain, & Tanaka, 1998). One interpretation of this holistic effect is that it represents a failure of selective attention, whereby subjects are unable to filter out irrelevant aspects of a face because of an attentional window that is applied over a large spatial area. Gauthier and Tarr (2002) showed that this ������holistic-inclusive������ effect is not specific to faces, but develops with perceptual expertise. They trained sub- jects to identify a novel set of homogeneous objects (Greebles). Subjects were considered to be Greeble experts when their reaction times were equivalent for verifying Greeble labels at both superordinate (family) and subordinate (individual) levels. Development of the holistic-inclusive effect occurred gradually over the course of training, becoming evident first for features that were close to one another, and later for more distal features, suggesting a widening window of spatial atten- tion. Furthermore, Gauthier and Tarr found that the de- velopment of holistic-inclusive processing for Greebles was correlated with changes taking place in the right Bukach et al. 49
fusiform face area (FFA), an extrastriate region that is typically more active for faces than for other object classes (Kanwisher, McDermott, & Chun, 1997 McCarthy, Puce, Gore, & Allison, 1997 Puce, Allison, Gore, & McCarthy, 1995 Haxby et al., 1994 Sergent & Signoret, 1992a). A third factor that is associated with the expert recognition of faces is the encoding of spatial relations between features. Spatial distances between features are particularly diagnostic for faces because all faces share a common global configuration of features (e.g., eyes above nose, nose above mouth). Whereas this global configuration, independent of finer spatial rela- tions, is important for recognizing faces at the basic level (recognizing an image as a face, as opposed to some other object), subtle variations in the distance between features is important for more specific judg- ments of faces. The mechanisms responsible for the encoding of spatial relations are generally referred to as ������configural processes.������ Evidence for expert configural processing of faces is based in part on the finding that the recognition of individual features (e.g., ������Emile���s eyes������) is superior when faces are presented in their original configuration relative to a novel configuration (the same eyes moved apart). Furthermore, this sensi- tivity to spatial configuration is attenuated when faces are inverted (Tanaka & Sengco, 1997). The disruption of configural processing with inversion is interpreted as a marker of expert configural processing (Diamond & Carey, 1986), and is often measured relative to the disruption of other types of local feature processing. This relative measure is known as the ������face inversion effect" (FIE). Using this FIE measure, researchers have found that sensitivity to changes in the spatial relations between features (e.g., distance between the eyes) is disproportionately disrupted relative to sensitivity to changes in local feature information (e.g., size, color, texture, or shape of the eyes themselves) when faces are inverted (Leder & Bruce, 1998, 2000 Searcy & Bartlett, 1996). Although the inversion effect was first thought to be unique to faces (Yin, 1969), Diamond and Carey (1986) demonstrated that similar inversion effects could be found for objects other than faces, providing the subject was an expert (e.g., dog experts show an inversion effect for dogs). Similarly, configural effects emerge with expert Greeble training (Gauthier & Tarr, 1997, 2002 Gauthier, Williams, Tarr, & Tanaka, 1998). Fine-level discrimination, holistic processing, and con- figural processing are all factors that have been identi- fied as particularly relevant to face recognition and perceptual expertise for objects in general. Although these processes are not likely to represent an exhaustive list of face recognition mechanisms, they nonetheless embody the beginnings of an a priori theoretical frame- work from which to consider impairments of general expertise processes that might result in what appears to be a selective deficit for face recognition. Impairment to any of these processes may disrupt face recognition, and thus, each factor may represent a different possible functional locus for prosopagnosia. In this context, we document a case of severe proso- pagnosia, L. R., who is unusual both in regard to the nature and locus of the injury leading to his impair- ment, and also in his impressive ability to identify visual objects other than faces. We systematically investigated each of the three factors identified above as critical to expert face recognition (Experiments 1���3). Surprisingly, we found that L. R. shows all three of the abilities associated with expert face recognition: L. R. can make fine-level discriminations, shows holistic-inclusive ef- fects, and shows a robust FIE. However, the spatial extent over which L. R. is able to apply these expert processes is limited. Experiment 4 confirmed that when feature and spatial changes are restricted to local regions of the face, L. R.���s expertise effects are limited to a single region, typically the lower region of the face. We discuss these findings in relation to mechanisms involved in expert face processing and perceptual expertise more generally. Case Description L. R. is a 49-year-old man who was involved in a motor vehicle accident in 1974, during which he was thrown from the front passenger seat of a truck onto the gearshift. The gear lever was missing the usual plastic cap covering the top, and L. R. received a penetrating head wound when the hollow metal tube of the un- capped gear shaft impaled his lower left cheek in front of the jaw, passing through the left intracranial cavity and sphenoid sinus. The shaft then entered the right cavernous sinus, clipping the right internal carotid artery and injuring the abducens nerve and the ophthalmic and maxillary divisions of the trigeminal nerve. It then pierced the right temporal lobe, leaving a bone fragment in the superficial aspect of the middle temporal gyrus. L. R. subsequently developed a right temporal intra- cerebral hematoma which was relieved through surgery, and also required clipping of the right internal carotid artery. CT scans revealed ablation of the anterior and inferior sections of the right temporal lobe, affecting the amygdala, but apparently sparing posterior regions, including the fusiform gyrus (see Figure 1). As a result of the clip, MRI is not possible. Visual acuity a year following the accident was 20/20 in both eyes with corrective lenses, and visual fields were full. Outward movement of his right eye is somewhat restricted due to right ocular motor nerve palsy. L. R. continues to have problems with depth perception, which he resolves by moving his head. His major residual complaint is that he can no longer recognize faces. He claims to rely primarily on distinctive features and context. For example, he has difficulty recognizing 50 Journal of Cognitive Neuroscience Volume 18, Number 1