Event-Related Brain Potentials Distinguish Processing Stages Involved in Face Perception and Recognition
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Clinical Neurophysiology 111 (2000) 694±705 www.elsevier.com/locate/clinph Event-related brain potentials distinguish processing stages involved in face perception and recognition Martin Eimer* Department of Experimental Psychology, University of Cambridge, Downing Street, Cambridge CB2 3EB, UK Accepted 15 October 1999 Abstract Objectives: An event-related brain potential (ERP) study investigated how different processing stages involved in face identi®cation are re¯ected by ERP modulations, and how stimulus repetitions and attentional set in¯uence such effects. Methods: ERPs were recorded in response to photographs of familiar faces, unfamiliar faces, and houses. In Part I, participants had to detect infrequently presented targets (hands), in Part II, attention was either directed towards or away from the pictorial stimuli. Results: The face-speci®c N170 component elicited maximally at lateral temporal electrodes was not affected by face familiarity. When compared with unfamiliar faces, familiar faces elicited an enhanced negativity between 300 and 500 ms (`N400f') which was followed by an enhanced positivity beyond 500 ms post-stimulus (`P600f'). In contrast to the `classical' N400, these effects were parietocentrally distrib- uted. They were attenuated, but still reliable, for repeated presentations of familiar faces. When attention was directed to another demanding task, no `N400f' was elicited, but the `P600f' effect remained to be present. Conclusions: While the N170 re¯ects the pre-categorical structural encoding of faces, the `N400f' and `P600f' are likely to indicate subsequent processes involved in face recognition. Impaired structural encoding can result in the disruption of face identi®cation. This is illustrated by a neuropsychological case study, demonstrating the absence of the N170 and later ERP indicators of face recognition in a prosopagnosic patient. q 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Face perception; Face recognition; Semantic processes; Attention; N400; Event-related brain potential 1. Introduction sulcus (cf. Perrett et al., 1982). The con®guration of face components is critical for many of these cells, as their activ- The ability to recognise familiar faces is a complex ity is reduced when face components are rearranged, or only achievement. Different lines of evidence suggest that face single face component are presented (Desimone et al., identi®cation processes are qualitative different from 1984). Based on fMRI recordings from human participants, processes underlying the identi®cation of non-face objects. Kanwisher et al. (1997) identi®ed an area in the fusiform Face recognition is more impaired than object recognition gyrus that was activated when faces were presented, but not when line drawings are presented instead of photographs in response to houses, scrambled faces, or hands. Perhaps (Davies et al., 1978), and is more affected by stimulus inver- the most convincing case for face-speci®c processing sion (Yin, 1969; Valentine, 1988). According to Farah modules comes from double dissociations between face (1991), object recognition is primarily based on representa- and object recognition. In prosopagnosia, face recognition tions where objects are decomposed into constituent parts, is disproportionally impaired, so that in the most extreme whereas face recognition depends on `holistic' representa- cases, object recognition capabilities seem entirely unaf- tions. Findings from neurophysiology also suggest func- fected (Sergent and Signoret, 1992; McNeil and Warring- tional and anatomical differences between face and object ton, 1993). In contrast, other patients are unable to identify recognition. Face-speci®c cells that respond strongly to different types of non-face objects, while their face recogni- faces, but not to other types of objects have been found in tion ability is remarkably spared (McCarthy and Warring- the macaque temporal cortex in the inferior temporal gyrus ton, 1986; Moscovitch et al., 1997). and on the banks and the ¯oor of the superior temporal If the identi®cation of faces is subserved by specialised processes, this should also be re¯ected in face-speci®c modulations of event-related brain potentials (ERPs). Alli- * Tel.: 144-1223-333936; fax: 144-1223-333564. E-mail address: [email protected] (M. Eimer) son et al. (1994) recorded ERPs intracranially to faces and 1388-2457/00/$ - see front matter q 2000 Elsevier Science Ireland Ltd. All rights reserved. CLINPH 99671 PII: S1388-2457(99)00285-0 M. Eimer / Clinical Neurophysiology 111 (2000) 694±705 695 non-face stimuli and found a face-speci®c negative potential physiological correlates of face identi®cation processes, with a latency of about 200 ms in the left and right fusiform may however be present at longer latencies. Several and inferior temporal gyri. Electrical stimulation of these previous ERP studies have employed familiar faces as areas resulted in a temporary inability to name familiar stimuli, but were primarily interested in effects of immedi- faces. In a study by BoÈtzel et al. (1995), faces elicited a ate stimulus repetitions (Barrett et al., 1988; Barrett and midline positivity and an increased negativity at lateral Rugg, 1989; Bentin and McCarthy, 1994; Begleiter et al., temporal electrodes (T5, T6) around 160 ms after stimulus 1995). Barrett et al. (1988) found an enlarged N400 compo- presentation (see also George et al., 1996; Eimer, 1998, nent when a familiar face did not match the identity of its 2000, for similar results). Bentin et al. (1996) found that predecessor. In the Bentin and McCarthy (1994) study, the faces elicited a negative potential with a latency of 170 N400 elicited by immediate repetitions of familiar and unfa- ms (N170) at lateral posterior temporal sites and a fronto- miliar faces was reduced in amplitude relative to the ®rst central positivity of slightly longer latency. No N170 was presentation of these stimuli. Only one very recent study triggered by cars, hands, furniture, or by scrambled faces. directly investigated ERP correlates of face recognition. While these ERP results support the idea that the proces- Bentin and Deouell (2000) found an enhanced negativity sing of face stimuli is based on specialised brain mechan- for familiar relative to unfamiliar faces in the N400 time isms, it is not clear which processing stages are re¯ected by range which they tentatively interpreted as indicating the these effects. In their in¯uential model of face recognition, activity of face recognition and identi®cation mechanisms. Bruce and Young (1986) distinguish between a perceptual Notably, no effect of familiarity on the N170 component structural encoding stage, where individual face features was found in this study, which led Bentin and Deouell and their spatial con®guration are analysed, and a subse- (2000) to conclude that this component re¯ects perceptual quent recognition stage, where structural representations stages of structural analysis that are not in¯uenced by face are compared with stored face representations (face recog- identi®cation processes. The aim of the present study was to nition units). When these units are suf®ciently activated due provide further insight into which processing stages are to their match with a structural representation, person iden- re¯ected by ERP modulations sensitive to faces, when and tity nodes in semantic memory can be accessed, resulting in how face identi®cation processes affect ERP waveforms, face identi®cation. and whether stimulus repetitions and attentional factors Bentin et al. (1996) obtained the face-speci®c N170 in¯uence ERP effects related to the familiarity of face components not only to intact upright faces, but also to stimuli. ERPs were recorded to familiar faces, unfamiliar inverted faces or isolated eyes (but see Eimer (1998)), and faces, and non-faces (houses). To determine whether parti- argued that the N170 is likely to re¯ect face-speci®c struc- cipants were able to successfully identify the faces declared tural encoding processes prior to processing stages involved as familiar, a familiar face/unfamiliar face discrimination in face identi®cation. Additional evidence for a link block was run at the end of the experiment. between the N170 and structural encoding of faces comes In Part I, photographs of familiar faces, unfamiliar faces, from a recent study by Eimer and McCarthy (1999), who and houses were presented in random order, and participants recorded ERPs to face and non-face stimuli from a severely had to respond to infrequently presented target stimuli prosopagnosic patient (see Bentin et al. (1999), for a similar (hands). ERPs elicited by familiar and unfamiliar faces case). Patient PHD has a prosopagnosia affecting both levels and by non-faces were compared to ®nd out if and how of the face recognition system. He is impaired in the struc- face-speci®c ERP modulations are affected by face famil- tural and perceptual analysis of faces and is also impaired in iarity. More speci®cally, it was studied whether familiarity recognising and identifying familiar faces. He shows would have no in¯uence on the N170 component (as substantial prosopagnosic de®cits in everyday life as well suggested by Bentin and Deouell (2000)), but would affect as in neuropsychological tests (see Eimer and McCarthy later parts of the ERP waveforms. Familiar and unfamiliar (1999), for details). He often fails to recognise highly famil- faces were presented repeatedly (immediate stimulus repe- iar faces including those