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Activation of Fusiform Face Area by Greebles Is Related to Face Similarity but Not Expertise

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Activation of Fusiform Face Area by Greebles Is Related to Face Similarity but Not Expertise Marijke Brants, Johan Wagemans, and Hans P. Op de Beeck Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/23/12/3949/1776974/jocn_a_00072.pdf by guest on 18 May 2021 Abstract ■ Some of the brain areas in the ventral temporal lobe, such sessions at identifying Greebles. We scanned participants be- as the fusiform face area (FFA), are critical for face perception fore and after training and examined responses in FFA and lat- in humans, but what determines this specialization is a mat- eral occipital complex. Most importantly and in contrast to ter of debate. The face specificity hypothesis claims that faces previous reports, we found a neural inversion effect for Greebles are processed in a domain-specific way. Alternatively, the ex- before training. This result suggests that people process the pertise hypothesis states that the FFA is specialized in pro- “novel” Greebles as faces, even before training. This prediction cessing objects of expertise. To disentangle these views, some was confirmed in a postexperimental debriefing. In addition, previous experiments used an artificial class of novel objects we did not find an increase of the inversion effect for Greebles called Greebles. These experiments combined a learning and in the FFA after training. This indicates that the activity in the fMRI paradigm. Given the high impact of the results in the lit- FFA for Greebles does not depend on the degree of expertise ac- erature, we replicated and further investigated this paradigm. In quired with the objects but on the interpretation of the stimuli as our experiment, eight participants were trained for ten 1-hr face-related. ■ INTRODUCTION 1997). Third, brain imaging experiments have found neu- Substantial evidence supports a dissociation between face ral responses that are highly specific to faces (Kanwisher perception and general object recognition, but what deter- & Yovel, 2006; Kanwisher, McDermott, & Chun, 1997). mines this dissociation is a matter of debate. Domain- The fusiform face area (FFA), a cortical region in the ven- specific hypotheses attribute this dissociation to the special tral temporal lobe, is activated at least twice as strongly status of faces per se (Kanwisher, 2000), whereas process- when subjects view faces than when they view any other specific hypotheses attribute this dissociation rather to class of visual stimuli yet tested (Kanwisher et al., 1997). the differential involvement of perceptual or cognitive Several researchers also found a weak inversion effect processes that are not necessarily specific to faces (Tarr in the FFA: a stronger activation for upright than for in- & Gauthier, 2000). Here, we implement one of the major verted faces (Yovel & Kanwisher, 2004, 2005). Fourth, sin- paradigms used to argue in favor of process-specific hy- gle unit recordings in monkeys have revealed a clustered potheses: laboratory training with Greebles. We show that population of cells in the temporal cortex that respond the neural signature of this training is actually most con- selectively to faces (see Tsao & Livingstone, 2008, for an sistent with domain-specific hypotheses. overview), suggesting a role for these cells in face recog- Evidence for dissociations between face perception nition (Afraz, Kiani, & Esteky, 2006). and generic object recognition comes from multiple para- There are at least two alternative hypotheses that try to digms. First, results from behavioral experiments indicate account for this dissociation between face and object rec- a different style of cognitive processing for faces (holistic ognition. The first hypothesis is the face specificity hypoth- processing) than for other objects (part-based process- esis, which states that cognitive and neural mechanisms ing). For example, effects of orientation inversion are underlying face perception are selectively engaged in per- more pronounced for faces than for other objects (Yin, ceptually processing faces and play little if any role in the 1969) and parts are particularly integrated into a whole perceptual analysis of nonface stimuli (Robbins & McKone, in upright faces (Maurer, Le Grand, & Mondloch, 2002; 2007; Duchaine & Nakayama, 2006; Duchaine, Yovel, Tanaka & Sengco, 1997; Tanaka & Farah, 1993). Second, Butterworth, & Nakayama, 2006; McKone, Kanwisher, & brain injury can produce selective deficits in face recog- Duchaine, 2006; McKone & Robbins, 2006; Moore, Cohen, nition while leaving object discrimination intact (Dricot, & Ranganath, 2006; Yue, Tjan, & Biederman, 2006; McKone Sorger, Schiltz, Goebel, & Rossion, 2008; Wada & Yamamoto, & Kanwisher, 2005; Xu, Liu, & Kanwisher, 2005; Yovel & 2001) and vice versa (Moscovitch, Winocur, & Behrmann, Kanwisher, 2005; Grill-Spector, Knouf, & Kanwisher, 2004; Rhodes, Byatt, Michie, & Puce, 2004; Carmel & Bentin, University of Leuven (K.U. Leuven), Belgium 2002; Kanwisher, 2000). © 2011 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 23:12, pp. 3949–3958 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00072 by guest on 29 September 2021 The second hypothesis, the expertise hypothesis, claims are some problems with this conclusion. First, they mostly that mechanisms for face processing are not engaged only examined changes of brain activation in face-selective re- by faces but are also applied in expert within-class discrimi- gions. Therefore, this study lacks a critical test for the ex- nation of nonfaces (McGugin & Gauthier, 2010; Curby, pertise hypothesis: Are the training effects specific to the Glazek, & Gauthier, 2009; Harley et al., 2009; Wong, Palmeri, FFA? Second, Greebles have a high degree of structural & Gauthier, 2009; Gauthier & Bukach, 2006; Gauthier, Curby, similarity to faces and body combinations. Therefore, a Skudlarski, & Epstein, 2005; Xu, 2005; Rossion, Curran, & small expertise effect (including a positive correlation be- Gauthier, 2002; Gauthier, Skudlarski, Gore, & Anderson, tween FFA activity and holistic processing) for Greebles 2000; Tarr & Gauthier, 2000; Gauthier, Behrmann, & Tarr, could reflect a specialized face-processing mechanism learn- 1999; Gauthier & Tarr, 1997). According to this hypothe- ing to stretch its definition of a face rather than a generic Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/23/12/3949/1776974/jocn_a_00072.pdf by guest on 18 May 2021 sis, face perception is special because we had a lifetime ex- expertise effect that could occur for any object class. Third, perience discriminating individual faces but almost no there are some methodological issues with this study (e.g., experience at making similar within-class discrimination the use of only five participants in their fMRI experiment; with other objects. Thus, faces are indeed processed in a for an overview, see McKone & Kanwisher, 2005). special manner, but the mechanisms carrying out that pro- Given these concerns, combined with the prominent cessing can work on other object classes given enough status and high impact of this earlier report in the litera- experience. This expertise hypothesis predicts that, when ture, we conducted a replication study of the fMRI Greeble we develop enough expertise in within-class object dis- training experiment (Gauthier & Tarr, 2002; Gauthier, crimination, the same mechanisms will be engaged in the Tarr, et al., 1999) with some important adjustments. First, processing of faces and of objects-of-expertise. Thereby, we also included the lateral occipital complex (LOC; the experts with nonface objects should also show the hall- area that mainly processes objects) in our analyses to ex- marks that usually differentiate face processing from object amine if there are any or even stronger changes in brain processing: objects of expertise should also be processed activation due to training beside the training effects found holistically and engage face-specific neural mechanisms. in FFA. We chose this region because other researchers To test the predictions of the expertise hypothesis, one (Op de Beeck, Baker, DiCarlo, & Kanwisher, 2006; Yue important approach has been to test laboratory-trained et al., 2006) already found training effects in LOC, but subjects using an artificial class of novel objects called not in FFA. Second, we manipulated the context in which Greebles (see Figure 1). Participants were trained to iden- the stimuli were introduced during training. With this tify different Greebles over several sessions (8–10 hr of manipulation, we tried to influence the interpretation of training). Gauthier, Tarr, Anderson, Skudlarski, and Gore the stimuli as living things (with faces) or artifacts/tools. (1999) have examined brain activations before, during, A potential role of stimulus interpretation was suggested and after Greeble training to monitor changes in the neu- post hoc by Op de Beeck et al. (2006) because they ob- ral substrates thought to mediate perceptual expertise, served one subject in their study that interpreted the more specifically the FFA. Their results showed that activa- trained stimuli (artificially created stimuli referred to as tion in the right FFA for upright minus inverted Greebles “smoothies”) as faces (reported in the postexperimental increased throughout Greeble training. This indicates that debriefing), and only this subject showed a training-related the inversion effect (a hallmark of holistic processing) increase in FFA activity. Here, we manipulated
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