Fusiform gyrus face-selectivity reflects facial recognition ability

Regions of the occipital and temporal lobes, including a region in the fusiform gyrus (FG), have been proposed to comprise a “core” visual representation system for faces, in part because they show face selectivity and face repetition suppression. But recent fMRI studies of developmental prosopagnosics (DPs) raise questions about whether these measures relate to face processing skills. Although DPs manifest deficient face processing, most studies to date have not shown unequivocal reductions of functional responses in the proposed core regions. We scanned 15 DPs and 15 non-DP control participants with fMRI while employing factor analysis to derive behavioral components related to face identification or other processes. Repetition suppression specific to facial identities in FG or to expression in FG and STS did not show compelling relationships with face identification ability. However, we identified robust relationships between face selectivity and face identification ability in FG across our sample for several convergent measures, including voxel-wise statistical parametric mapping, peak face selectivity in individually defined “fusiform face areas” (FFAs), and anatomical extents (cluster sizes) of those FFAs. None of these measures showed associations with behavioral expression or object recognition ability. As a group, DPs had reduced face-selective responses in bilateral FFA when compared with non-DPs. Individual DPs were also more likely than non-DPs to lack expected face-selective activity in core regions. These findings associate individual differences in face processing ability with selectivity in core face processing regions. This confirms that face selectivity can provide a valid marker for neural mechanisms that contribute to face identification ability. Developmental prosopagnosia (DP) is a condition in which individuals (DPs) with otherwise normal vision, intelligence, and social functioning show face recognition impairments in the absence of evident brain injury. Although numerous behavioral studies have enhanced understanding of the cognitive bases of DP (Bentin, Degutis, D’Esposito, & Robertson, 2007; Humphreys, Avidan, & Behrmann, 2007; Duchaine & Nakayama, 2006b; Behrmann, Avidan, Marotta, & Kimchi, 2005), progress on the neural basis of DP is more limited to date, with the few existing studies of this reviewed below. An influential account of the functional neuroanatomy of face perception (Haxby, Hoffman, & Gobbini, 2000) describes a so-called core system in the occipital and temporal lobes. These core regions are considered responsible for visual recognition of facial attributes (Haxby et al., 2000) and are distinguished from a more “extended system,” which further processes information resulting from visual recognition. The proposed “core” regions have @2011 Massachusetts Institute of Technology Corresponding author: Nicholas Furl, National Institutes of Health, Building 49, 1B80, 49 Convent Dr, Bethesda MD, USA, phone: 301-496-5625, furlno@mail.nih. gov. Europe PMC Funders Group Author Manuscript J Cogn Neurosci. Author manuscript; available in PMC 2012 April 10. Published in final edited form as: J Cogn Neurosci. 2011 July ; 23(7): 1723–1740. doi:10.1162/jocn.2010. 21545. E uope PM C Fuders A uhor M ancripts E uope PM C Fuders A uhor M ancripts been associated with face selectivity: they typically respond more strongly to faces than to nonface objects (cf. Yovel & Kanwisher, 2005). Neural responses in core regions can also attenuate in response to repeated facial information (i.e., repetition suppression). In normal observers, identity repetition typically suppresses regions in the fusiform gyrus (FG) while repeating more changeable attributes, such as expression, typically leads to BOLD suppression in other regions such as STS (e.g., see Fox, Moon, Iaria, & Barton, 2009; Rotshtein, Henson, Treves, Driver, & Dolan, 2005; Andrews & Ewbank, 2004; Winston, Henson, Fine-Goulden, & Dolan, 2004). Although these core face-related brain regions suggest possible loci for neural deficits in DPs, there is scant evidence to date showing functional deficits in these regions. DP case studies using fMRI have mainly reported relatively normal face-selective responses in FG (e.g., see Minnebusch, Suchan, Köster, & Daum, 2009; Thomas et al., 2008; Behrmann, Avidan, Gao,& Black, 2007; Williams, Berberovic, & Mattingley, 2007; Avidan, Hasson, Malach, & Behrmann, 2005; Hasson, Avidan, Deouell, Bentin, & Malach, 2003). Despite these numerous “null” (i.e., apparently normal) findings, some atypical findings in individual cases have been identified, including some DPs with no face selectivity (Minnebusch et al., 2009; Bentin et al., 2007; Hadjikhani & de Gelder, 2002), weakened face selectivity (Avidan & Behrmann, 2009), or expression dependent FG face selectivity (van de Stock, van de Riet, Righart, & de Gelder, 2009). One study (using an unusually large sample of DPs) found that voice recognition deficits in DPs were associated with reduced face selectivity in core regions (von Kriegstein et al., 2008). Studies examining repetition suppression have reported apparently normal suppression to repeated (familiar) faces in DPs (Avidan et al., 2005, 2009; Williams et al., 2007). Thus, functional imaging of DP has provided inconsistent or incomplete evidence for substantially altered neural function in the “core” regions that have been associated with face processing in studies of people with typical face skills. But such evidence might still be reconciled with a role for these core regions in DP if, for example, face related effects were reduced or variable in DPs rather than being completely abolished. It remains possible that the magnitude of functional abnormalities might relate systematically to the extent of reduced face skills. Indeed one open possibility, which has not been rigorously investigated to date, is that DPs might constitute the lower tail of a fairly continuous distribution of face identification ability. If so, one would not predict discrete, all-or-nothing functional deficits that should be easily observed in every individual DP. Instead, one would predict functional neuroanatomic correlates of performance might be best detected by testing for continuous relationships between fMRI measures and a wide range of behavioral face identification ability across both DPs and individuals exhibiting normal variation in face skills. Here, we aimed to implement such an “individual differences” approach by testing not only a sample large enough to allow conventional group contrasts (DPs vs. non-DPs) but also a more systematic analysis of neuroimaging data in relation to the subject-by-subject scores on a battery of tests. We recently applied this approach successfully in a purely structural MRI analysis of 17 DPs and 18 non-DP comparison participants (Garrido et al., 2009). We tested these participants with a battery of behavioral tasks assessing judgments of facial identity, facial expression, and nonface object recognition. Using factor analysis, we showed that we could derive summary scores for orthogonal components of behavioral performance from this battery. Empirically, this yielded separate face identity, face expression, and nonface object behavioral components. In our MRI morphometric analysis, these factor scores showed linear relationships with gray matter volume in temporal cortex across the entire sample (Garrido et al., 2009). Using the same factor analytic approach to individual differences in behavioral performance, we now extend our analysis of this sample by exploring the relationship of face Furl et al. Page 2 J Cogn Neurosci. Author manuscript; available in PMC 2012 April 10. E uope PM C Fuders A uhor M ancripts E uope PM C Fuders A uhor M ancripts identification performance deficits to the aforementioned fMRI measures of functional face selectivity and repetition suppression. We hypothesized that the use of these measures may reveal hitherto undiscovered relationships between face identification ability and fMRI signal in the core face-related brain regions, such as FG.