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Pdf/22/10/2289/1770340/Jocn.2009.21320.Pdf by Guest on 18 May 2021 Characterizing the Spatio-temporal Dynamics of the Neural Events Occurring prior to and up to Overt Recognition of Famous Faces Boutheina Jemel1, Anne-Marie Schuller2, and Valérie Goffaux3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/10/2289/1770340/jocn.2009.21320.pdf by guest on 18 May 2021 Abstract ■ Although it is generally acknowledged that familiar face recog- of familiar faces. Although the N170 and the N250 face-sensitive nition is fast, mandatory, and proceeds outside conscious control, responses displayed an abrupt activity change at the moment of it is still unclear whether processes leading to familiar face recog- overt recognition of famous faces, later ERPs encompassing the nition occur in a linear (i.e., gradual) or a nonlinear (i.e., all-or- N400 and late positive component exhibited an incremental in- none) manner. To test these two alternative accounts, we recorded crease in amplitude as the point of recognition approached. In scalp ERPs while participants indicated whether they recognize addition, famous faces that were not overtly recognized at one as familiar the faces of famous and unfamiliar persons gradually trial before recognition elicited larger ERP potentials than unfamil- revealed in a descending sequence of frames, from the noisier to iar faces, probably reflecting a covert recognition process. Overall, the least noisy. This presentation procedure allowed us to charac- these findings present evidence that recognition of familiar faces terize the changes in scalp ERP responses occurring prior to and implicates spatio-temporally complex neural processes exhibit- up to overt recognition. Our main finding is that gradual and all- ing differential pattern activity changes as a function of recogni- or-none processes are possibly involved during overt recognition tion state. ■ INTRODUCTION The functional model put forward by Bruce and Young Many of our everyday behaviors, such as recognizing (1986) has promoted the idea that face familiarity takes acquaintances in the street, reading a book, appropriately place at the level of face-specific representation, referred to manipulating objects, and so forth, appear to be discon- as face recognition units (FRUs) that store structural per- certingly effortless and automatic. For instance, we cannot ceptual information of familiar faces. When the visual input look at a face and decide whether or not we recognize it; from a perceived face matches its stored representation, no matter how hard we try. Face recognition is fast, man- the corresponding FRU is activated, therefore generating datory, and proceeds outside conscious control (Bruce & a feeling of familiarity. FRUs are viewed as transmitting a Young, 1986). This phenomenon and a number of other graded signal that is proportional to the degree of resem- observations have been taken as evidence that face recog- blance between stored representation and the current nition may be achieved in an all-or-none fashion. Paradoxi- percept (Bruce & Young, 1986). FRU activation, in turn, in- cally, other everyday situations like the types of slips and stigates the access to all sorts of identity-specific and seman- errors in recognizing faces and several empirical findings tic information (person–identity nodes, PINs) about the from laboratory experiments (Hay, Young, & Ellis, 1991; face, and finally, retrieval of his or her name. Moreover, in Young, Hay, & Ellis, 1985) strongly suggest that several Burton et al.ʼs (1990) model, face recognition is supported states of face recognition are possible and that the under- by thresholded devices located at PINs, the activation of lying mechanisms would operate in a continuous and which rapidly triggers retrieval of associated person-specific graded manner. These two views have been conceptualized information. Accordingly, these PINs operate in an “all-or- in theoretical frameworks of face recognition (Burton, none” (i.e., binary) fashion (Burton et al., 1990); if their Bruce, & Johnston, 1990; Bruce & Young, 1986) but there signal strength exceeds a set threshold criterion, then a is as yet no clear-cut evidence for an all-or-none or a gradual recognition response is given, and if it is below threshold, account of the process underlying familiar face recognition. the face is judged as unfamiliar. Based on these two models, face recognition entails two memory processes that might be related but are, by no 1Université de Montréal, Canada, 2Public Research Center for means, synonymous. The first computes similarity of probe Health, Department of Public Health, Luxemburg, 3University faces to stored traces in long-term memory and generally of Maastricht, The Netherlands refers to a diffuse and undifferentiated feeling of familiarity, © 2009 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:10, pp. 2289–2305 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2009.21320 by guest on 02 October 2021 that is, a general, context-free sense of knowing that a given over lateral occipito-temporal recording sites, known as face has been encountered at some time in the past (i.e., the N170 face-sensitive component (Bentin, Allison, Puce, Bruce & Young, 1986). The second generally refers to Perez, & McCarthy, 1996). The demonstration that the explicit forms of memory retrieval of specific person iden- N170 is highly sensitive to stimulus manipulations that tity information (Burton et al., 1990), that is, a context- impede perceptual face processing ( Jemel, Schuller, dependent process associated with the experience of not et al., 2003; Rossion et al., 2000; George, Evans, Fiori, only knowing that a face is familiar but also remembering Davidoff, & Renault, 1996) and is not sensitive to memory- some relevant information that allow identification of that related and familiarity-related factors (Tanaka et al., 2006; face. Accordingly, one can argue that face familiarity is a Schweinberger et al., 2002; Bentin & Deouell, 2000; Eimer, memory process that supports recognition without being 2000) provided support for the claim that this ERP com- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/10/2289/1770340/jocn.2009.21320.pdf by guest on 18 May 2021 necessarily accompanied by conscious retrieval of detailed ponent reflects a fairly early stage of the visual analysis of memories (Mandler, 1980). Evidence for this argument faces. Other lines of research, however, showed reliable mainly comes from neuropsychological studies on proso- effects of familiarity, repetition priming, and recogni- pagnosia, a face recognition impairment caused by selective tion on N170 responses to faces ( Jemel, Pisani, Rousselle, damage in ventral occipito-temporal cortex and anterior Crommelinck, & Bruyer, 2005; Tanskanen, Näsänen, temporal regions (Damasio, Tranel, & Damasio, 1990). De- Montez, Päällysaho, & Hari, 2005; Jemel, Pisani, Calabria, spite the failure in overt or conscious recognition of famil- Crommelinck, & Bruyer, 2003; Caharel et al., 2002), sug- iar faces, residual effects of facial familiarity can still be gesting that as early as 170 msec after stimulus onset, the demonstrated in some prosopagnosic patients through brain is individuating previously encoded faces. a variety of indirect measures that do not depend on ex- Nonetheless, there is now an increasing number of plicit recognition (Young, 1994), such as implicit learn- studies showing that the earliest time epoch at which ingoftrueanduntrueface–name associations (Bruyer familiar and unfamiliar face ERPs differ occurs circa 200– et al., 1983), semantic priming (Barton, Cherkasova, & 300 msec after stimulus onset, at the level of an occipito- Hefter, 2004), eye movement scan paths (Rizzo, Hurtig, & temporal negative potential known as the N250 (Begleiter, Damasio, 1987), as well as electrophysiological (Renault, Porjesz, & Wang, 1995); N250 familiarity effect typically Signoret, Debruille, Breton, & Bolgert, 1989) and skin- takes the form of enhanced negative potentials in response conductance response measures [SCR] (Tranel & Damasio, to familiar than to unfamiliar faces (Tanaka et al., 2006; 1985). Moreover, the reverse dissociation, that is, explicit Schweinberger, Pfütze, & Sommer, 1995). This result has recognition without familiarity, has been supported by led some authors to suggest that this component reflects some evidence in patients with ventromedial frontal dam- the activation of preexistent internal representation within age (see Tranel, Damasio, & Damasio, 1995) and in pa- the face recognition system (Bruce & Young, 1986). How- tients with delusional misidentification syndromes such as ever, studies investigating repetition effects within the time Capgras delusion (Ellis, Young, Quayle, & DePauw, 1997; range of the N250 (i.e., N250r for repetition) have cast Hirstein & Ramachandran, 1997). Tranel et al. (1995) re- some doubt on this interpretation. Most notably, larger ported the case of some patients with ventromedial frontal N250r for repeated as compared to nonrepeated faces have damage who failed to show discriminatory autonomic been reported for familiar and unfamiliar faces (Begleiter responses to familiar and unfamiliar faces that were other- et al., 1995; Schweinberger et al., 1995), although sometimes wise consciously recognized. Taken collectively, these sets with reduced amplitudes for unfamiliar faces (Herzmann, of findings suggest that the activation of face representation Schweinberger, Sommer, & Jentzsch, 2004). These find- is necessary
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