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Neural Correlates of Generic Versus Gender-Specific Face Adaptation

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Neural Correlates of Generic Versus Gender-Specific Face Adaptation Neural Correlates of Generic versus Gender-specific Face Adaptation Nadine Kloth1, Stefan R. Schweinberger1, and Gyula Kovács2,3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/10/2345/1770283/jocn.2009.21329.pdf by guest on 18 May 2021 Abstract ■ The perception of facial gender has been found to be adap- face exposure in general. We compared N170 effects after adap- tively recalibrated: adaptation to male faces causes participants tation to either male or androgynous faces. Additionally, we to perceive subsequent faces as more feminine and vice versa investigated cross-modal adaptation for the same test faces fol- [Webster,M.A.,Kaping,D.,Mizokami,Y.,&Duhamel,P. lowing male or androgynous voice adaptors. Visual adaptation Adaptation to natural facial categories. Nature, 428, 557–561, to face gender replicated previously reported aftereffects in clas- 2004]. In an event-related brain potential (ERP) study, Kovács sifying androgynous faces, and a similar trend was observed fol- et al. [Kovács, G., Zimmer, M., Banko, E., Harza, I., Antal, A., lowing adaptation to voice gender. Strikingly, N170 amplitudes & Vidnyanszky, Z. Electrophysiological correlates of visual were dramatically reduced for faces following face adaptors (rela- adaptation to faces and body parts in humans. Cerebral Cortex, tive to those following voice adaptors), whereas only minimal 16, 742–753, 2006] reported reduced N170 amplitudes and in- gender-specific adaptation effects were seen in the N170. By creased latencies for test faces following female gender adapta- contrast, strong gender-specific adaptation effects appeared in a tion compared to control stimulus (a phase randomized face) centroparietal P3-like component (∼400–600 msec), which in adaptation. We examined whether this N170 attenuation to test the context of adaptation may reflect a neural correlate of the faces was related to the adaptorʼs gender, or to adaptation to detection of perceptual novelty. ■ INTRODUCTION processing, even though they are similar in other respects Although the investigation of adaptation to simple stimu- to low-level adaptation effects, for instance, in time course lus attributes (e.g., motion or color) has a very long tra- (Kloth & Schweinberger, 2008; Leopold, Rhodes, Muller, & dition, it has been a striking novel discovery within the Jeffery, 2005). past decade that adaptive recalibration also governs the Of special interest for the present study are aftereffects in perception of very complex visual stimuli such as human the perception of facial gender. Following the prolonged faces. Webster and MacLin (1999) were the first to report viewing of a female (or male) face, participants tend to clas- visual aftereffects in face perception: They found that sify subsequently presented androgynous faces as distinc- adaptation to distorted (e.g., contracted) faces led to a tively male (or female; Webster et al., 2004), suggesting perception of veridical faces as being distorted in the that distinct neural populations selectively code aspects of direction opposite to the adaptor (e.g., expanded). Since femaleness and maleness in faces. In line with this idea, then, similar contrastive aftereffects have been reported it has been shown more recently that simultaneous oppo- to follow adaptation to facial identity (Löffler, Yourganov, site aftereffects of adaptation can be elicited for male and Wilkinson, & Wilson, 2005; Leopold, OʼToole, Vetter, & female faces (Bestelmeyer et al., 2008; Little, DeBruine, & Blanz, 2001), eye gaze direction ( Jenkins, Beaver, & Jones, 2005). Calder, 2006; Seyama & Nagayama, 2006), viewpoint Despite the large number of studies investigating the (Fang, Ijichi, & He, 2007), ethnicity (Webster, Kaping, nature of behavioral aftereffects, the neural correlates of Mizokami, & Duhamel, 2004), and emotional expression human face adaptation are only beginning to be investigated (Butler, Oruc, Fox, & Barton, 2008; Fox & Barton, 2007; by electrophysiological and functional imaging methods Webster et al., 2004). Such high-level visual aftereffects (Kovács, Cziraki, Vidnyanszky, Schweinberger, & Greenlee, have been shown to be largely size invariant (e.g., Zhao 2008; Kovács et al., 2006). At the same time, when consider- & Chubb, 2001), suggesting that they do not mainly re- ing the substantial research studying ERPs in face percep- flect adaptation to single features on low levels of visual tion, the investigation of ERP correlates of face adaptation should provide important information; both with respect 1Friedrich-Schiller-University, Jena, Germany, 2University of to the stages of face processing that are affected by adap- Regensburg, Regensburg, Germany, 3Budapest University of tation and with respect to the level of neural processing Technology and Economics, Budapest, Hungary reflected in a specific component. © 2009 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:10, pp. 2345–2356 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2009.21329 by guest on 28 September 2021 The successful combination of face adaptation paradigms images). Not only did the control adaptor lack any gender- and ERP recordings is illustrated by Kovács et al. (2006), who specific information, it also lacked any shape-specific infor- investigated the electrophysiological correlates of gender mation characteristic of either faces or hands. In the present adaptation. This study focused on the face-sensitive N170 study, we aim at disentangling the respective influences of component (Bentin, Allison, Puce, Perez, & McCarthy, stimulus category repetition and gender adaptation on 1996), which is thought to be a correlate of the structural N170. Although we used the same test faces and a similar encoding of faces (Rossion et al., 2000; Bentin et al., 1996), experimental design as Kovács et al. (2006), we used an- andwhichwashypothesizedtobethemajorERPcompo- drogynous adaptor faces as control stimuli, which there- nent affected by selective adaptation to gender stimuli. fore should lack any adaptive power with respect to gender Further, Kovács et al. investigated high-level gender adapta- perception (cf. Webster & MacLin, 1999). Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/10/2345/1770283/jocn.2009.21329.pdf by guest on 18 May 2021 tion in the perception of human hands, and included cross- The most influential theoretical model (Bruce & Young, categorical adaptation conditions, as participants adapted 1986) makes little reference to neurophysiological pro- to photographs of female faces, female hands, or control cesses mediating various aspects of face perception, whereas stimuli (Fourier phase randomized versions of the adap- more recent models make an attempt to integrate ex- tors). In line with the findings by Webster et al. (2004), adap- perimental, electrophysiological, and neuroimaging findings tation to female faces as compared to control adaptation (e.g., Schweinberger & Burton, 2003; Haxby, Hoffman, & stimuli led to a bias to perceive subsequently presented Gobbini, 2000). In terms of these models, we expect the faces as more masculine. Interestingly, although hands ap- present study to be informative for the question of whether peared to be comparatively weaker cues for a personʼs gen- the N170 attenuation reflects adaptation at an early level of der, qualitatively similar adaptation effects were observed “face detection” (i.e., the detection of a generic facial con- for hands. By contrast, Kovács et al. did not find evidence figuration in early perceptual processing), or instead at a for cross-categorical aftereffects, strongly suggesting that more advanced stage of structural encoding of invariant gender adaptation effects are category-specific. Paralleling facial information about gender (cf. Haxby et al., 2000). these perceptual aftereffects, the analysis of the N170 re- A second aim of the present study was to test whether vealed that adaptation to both female hands and female the previously observed category specificity of the gender faces resulted in a strong attenuation of this component only adaptation effect (Kovács et al., 2006) would also hold for when adaptors were of the same category as test stimuli. an auditory–visual cross-modal condition. Whereas we are N170 amplitude to test stimuli was reduced, and latency in- unaware of strong reasons to expect a similar perceptual creased, after adaptation to faces and hands as compared to integration for faces and hands, our idea of an auditory– control stimuli. Consequently, the authors suggested this visual adaptation condition was prompted by recent evi- modulation as being the primary correlate of shape-selective dence for strong perceptual integration of faces and voices facial gender adaptation in humans. However, it is not im- (e.g., von Kriegstein et al., 2008), which is currently being mediately evident how this interpretation can be reconciled considered in models of person perception (Campanella & with other studies which found the N170 to be insensi- Belin, 2007). Of particular relevance, an auditory influence tive to facial gender processing (Mouchetant-Rostaing & on the perception of face gender was recently reported Giard, 2003; Mouchetant-Rostaing, Giard, Bentin, Aguera, by Smith, Grabowecky, and Suzuki (2007). In this study, & Pernier, 2000). androgynous faces were perceived as more male when Similar to the findings of Kovács et al. (2006), pronounced simultaneously combined with pure tones in the funda- effects of adaptation
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