During aging, the human brain undergoes various changes in structure, function, and neural transmission (Sowell et al., 2003; Raz et al., 2005). These alterations most probably underlie, and certainly covary with cognitive functioning (Cabeza et al., 2004; Dennis and Cabeza, 2008; Nyberg et al., 2012). During childhood, the interaction of maturation, experience, and learning results in cortical differentiation (for review, see Johnson, 2001; Scherf et al., 2007), which is paralleled by more fine-grained cognitive abilities (Li et al., 2004; Werkle-Bergner et al., 2009). This pattern reverses during older age, when senescent changes include cognitive and sensorimotor dedifferentiation (Lindenberger and Baltes, 1994; Baltes and Lindenberger, 1997; Lindenberger et al., 2001) and diminished cortical specialization (Park et al., 2004, 2012).

Critically, age-related alterations and their putative consequences can be very diverse, and within-cohort differences can be similarly pronounced as between-cohort differences (Salthouse, 2013). More specifically, while some older adults show decreased performance in memory and executive processes (for overview, see Anderson and Craik, 2000), others maintain high levels of functioning, and match (see e.g., Cabeza et al., 2002; Duarte et al., 2006; Friedman et al., 2010) or even outperform their younger counterparts (Christensen et al., 1999; Henry et al., 2004; Federmeier et al., 2010). Results from functional brain imaging suggest that different processes in the aging brain could mediate such performance differences: First, reduced activations of memory-related brain regions were found in older adults with poor performance (for review, see Grady, 2008). Second, increased activations in older participants were observed in prefrontal areas contralateral to those usually activated in younger adults (for reviews, see Cabeza, 2002; Park and Reuter-Lorenz, 2009; Reuter-Lorenz and Park, 2010; but see Nyberg et al., 2010, for potentially discrepant results from longitudinal data). Importantly, these latter findings were interpreted as indexing either dedifferentiation or compensation (for reviews, see Reuter-Lorenz and Cappell, 2008; Park and Reuter-Lorenz, 2009). While dedifferentiation connotes “negative plasticity” in terms of loss in specialization of neuro-cognitive structures, compensation connotes “positive plasticity,” allowing additional resource recruitment to optimize performance (Reuter-Lorenz and Park, 2010). This debate remains largely unresolved (Davis et al., 2012).

In line with the dedifferentiation view, several studies on object and face processing suggested the fading of distinctive neural representations with increasing age in ventral visual cortex. Of note, activation in fusiform gyrus, which is category-sensitive for faces in younger adults, was less selective in older adults (Park et al., 2004, 2012; Chee et al., 2006). Other studies used event-related potentials (ERPs) to examine the face-sensitive N170, a negative occipito-temporal peak at approximately 170 ms after stimulus onset (Bentin et al., 1996; Eimer, 2011) to elucidate age-related changes in face processing. At potential variance with the above-described neuroimaging results, N170 category-selectivity (with larger N170 to faces than objects) was similarly found across age groups (Gao et al., 2009; Daniel and Bentin, 2010), suggesting preserved neural sensitivity for faces in older adults¹. However, the N170 is sometimes increased in older adults (Gao et al., 2009; Daniel and Bentin, 2010; Wiese et al., 2013a; see also Rousselet et al., 2009, who reported larger amplitudes in older participants slightly after the N170 peak), and is also larger for inverted relative to upright faces, which is commonly interpreted as reflecting disrupted configural face processing. Notably, smaller N170 inversion effects were also observed in older participants (Gao et al., 2009; Daniel and Bentin, 2010). Hence, a larger N170 for upright faces and a smaller inversion effect in older adults may indicate a general reduction in early stages of face perception with higher age, potentially affecting subsequent higher-order cognitive functions, such as memory (see also Chaby et al., 2011). Consequently, the degree of preserved vs. deficient face perception in older adults might be reflected in differential face memory performance. To our knowledge, this idea has not been addressed in previous work.

The ability to distinguish between exemplars within a face category and to discriminate individual faces develops early, with a specialization toward own species faces from around 6 months of age (Pascalis et al., 2002) and subsequent further tuning toward own-race faces during childhood (see e.g., Scherf and Scott, 2012). In adults, the own-race bias (ORB) reflects the consistent finding of better memory for own-relative to other-race faces (for overview, see Meissner and Brigham, 2001). However, whether an ORB can still be observed in older adults has been scarcely investigated (Wallis et al., 2012). Age-related dedifferentiation could result in a less specialized face processing system (particularly in those older adults with poor face memory), and therefore in a reduced ORB, given that this effect is commonly interpreted to reflect expertise-related fine tuning of face processing mechanisms (Valentine and Endo, 1992; Tanaka et al., 2013). Here, we examined memory for own- and other-race faces in two groups of high- and low-performing older adults to test whether poor face memory in low-performers reflects advancing dedifferentiation (as indexed by a reduced or absent ORB). In addition, we addressed the question, whether reduced memory performance is associated with deteriorated perceptual processing as indexed by the N170.

Several recent studies have identified neural correlates of the ORB using ERPs, and N170 seems to play a prominent role in the generation of this effect. Suggestive of reduced early perceptual processing, other-race faces were found to elicit a larger N170 than own-race faces (Balas and Nelson, 2010; Stahl et al., 2010; Caharel et al., 2011). In a recent study, we reported a larger N170 to other-race faces during the learning phases of a recognition memory paradigm, in both young Asian and Caucasian participants (Wiese et al., 2014). Importantly, this effect during encoding significantly correlated with the subsequent recognition advantage for own-race faces during test. Apart from the ORB, an own-age bias (OAB) in terms of better memory for own-age relative to other-age faces has also been consistently described (for reviews, see Rhodes and Anastasi, 2012; Wiese et al., 2013b). To avoid underestimating older adults' performance, we decided to examine their face recognition memory in a full-factorial design by using young and old own- and other-race faces (Wiese, 2012).

The aim of our investigation was two-fold: First, we tested whether low- relative to high-performing participants would exhibit a reduced (or even absent) behavioral ORB which would argue for a (incipiently) dedifferentiated face processing system in this participant group. Second, we examined whether N170 effects would co-vary with memory performance, indicating less efficient early face perception in those older participants with lower memory performance.

The present study examined the ORB in face recognition memory in high- and low-performing older adults. Despite prominent overall performance differences, both groups demonstrated an equivalent magnitude of the ORB. Paralleling these behavioral results, ERP effects of face ethnicity first showed up in a larger N170 to young Asian vs. Caucasian faces in both groups alike. Additionally, performance-related ERP differences were observed between groups: While low-performing older adults showed a tendency for a right-lateralization of N170, this was not the case in high-performers. These findings are discussed in more detail below.

Our first aim was to test whether poor overall performance would be accompanied by dedifferentiation of processing within the category of faces, in terms of a reduced ORB in low-performers. Such a finding would complement previous reports of attenuated between-category (faces vs. objects) neural distinctiveness in older adults (Park et al., 2004, 2012), by indicating a degree of loss in the fine-tuning of the face processing system. We observed a clear ORB for young faces, which was virtually identical in both high- and low-performing participants. We therefore conclude that the fine-tuning of the face processing system of low-performers was not compromised when compared to high-performers, despite their reduced overall face memory. This conclusion is also in line with our finding of similar ethnicity effects in the N170 and the directly following time window in the two older groups (convergent with the additional result of no significant correlation of the ERP ethnicity effects with overall memory performance in both time segments), which further suggests similar encoding of facial race in the older groups.

Our observation of a preserved fine-tuning of the face processing system in older adults is generally in line with findings from an individual difference perspective. Hildebrandt et al. (2011) observed no dedifferentiation of individual differences in the latent constructs of face cognition as compared to general cognitive functioning. This finding was further substantiated in a subsequent study comparing object and face processing, in which only a slight dedifferentiation was observed, which was not specific for faces but operated on a more general cognitive level (Hildebrandt et al., 2013). In the present study, the behavioral ORB was equivalent between groups, although overall memory was reduced in low performers. Hence, we suggest that low performers did not exhibit poor face memory due to less specialized face processing, but rather due to more general cognitive decline.

Of note, although a previous study from our group found a significant correlation between the N170 ethnicity effect and the behavioral ORB (Wiese et al., 2014), two studies using a latent variable approach reported no relationship between the amplitude of the N170 and face cognition (Herzmann et al., 2010; Kaltwasser et al., in press). Yet, the latent variable approach produces combined measures of a number of tests, which may well tap into different processes than those reflected by N170 amplitude. More precisely, N170 is typically thought to represent very early perceptual processing stages (such as structural encoding or the detection of a face-like pattern, see e.g., Amihai et al., 2011; Eimer, 2011). Thus, less efficient processing of other-race faces at this early processing stage appears to result in a cascade of less efficient subsequent processes, which may ultimately result in less accurate recognition memory. Importantly, none of the tests used in the studies by Herzmann et al. (2010) or Kaltwasser et al. (in press) examined the processing of other-race faces. Early perceptual processing stages may have been highly efficient in all tasks used by Herzmann and others (Herzmann et al., 2010; Kaltwasser et al., in press), but not in the other-race conditions of the present and our previous study.

At a more specific level it is notable that ethnicity effects were prominent for young but not old faces, both in the N170 component and the subsequent time window, as well as in the behavioral ORB. The absence of an ORB for old faces in memory replicates two recent studies (Wallis et al., 2012; Wiese, 2012). We attribute this consistent absence of an ORB for old faces to decreased perceptual salience of ethnicity information in these faces, along with an increased salience of general age-related changes in facial shape and skin texture. The second aim was to examine whether the previously observed larger N170 amplitude in older as compared to young adults (e.g., Wiese et al., 2013a) was related to a decrease in early perceptual processing, which would in turn result in reduced face memory in older adults. This idea was based on the N170 inversion effect, reflecting an increased N170 amplitude for inverted, less configurally processed faces (e.g., Jacques et al., 2007), an effect which is reduced in older participants (Gao et al., 2009; Daniel and Bentin, 2010; Saavedra et al., 2012). In the present study, a decrease in face memory was not associated with larger N170 amplitudes, arguing against the idea of less efficient early face perception as the basis for reduced memory. If anything, N170 was larger in high- relative to low-performing participants, which, however, was apparent only over the left hemisphere.

Related to this latter finding, we detected a significant interaction involving the factors hemisphere and group, which suggested a more right-lateralized N170 in low-performers and a more bilateral pattern in high-performers. This finding was additionally confirmed in a correlation analysis, in which a more bilateral N170 was associated with higher overall performance. N170 is typically lateralized to the right hemisphere in young participants (e.g., Bentin et al., 1996; Amihai et al., 2011; Eimer, 2011), whereas a reduced lateralization of N170 amplitude in older adults has been previously described (Gao et al., 2009; Daniel and Bentin, 2010). Based on previous neuroimaging results (e.g., Cabeza, 2002; Cabeza et al., 2002) this finding has been interpreted as reflecting compensation of age-related decrements in face perception (Gao et al., 2009; Daniel and Bentin, 2010). The present study adds to this idea, by revealing that a reduced laterality of N170 can indeed relate to performance levels. Our finding is generally in line with the idea of reduced hemispheric asymmetry as a function of compensation rather than dedifferentiation (for reviews, see Cabeza, 2002; Reuter-Lorenz and Cappell, 2008). This may not only occur for higher-order cognitive processes, but also for (early) perceptual processes (De Sanctis et al., 2008) and the present findings extend this idea to the domain of face processing. However, although a similar pattern compared to the first half was observed, the interaction of hemisphere by group was no longer significant in the second half of the experiment, in which overall performance was clearly reduced in both groups. This finding may suggest that compensatory neural activity requires effortful processing and that fatigue hampers such activity in high performing older adults.

Although the more bilateral N170 in high-performers argues for a compensatory mechanism, the specific interpretation of their enhanced left-hemispheric N170 is subject to debate. One possibility considers that the left hemisphere may be more involved in feature-based than configural or holistic face processing (Rossion et al., 2000; Scott and Nelson, 2006). Accordingly, high-performers may engage in more feature-based processing during encoding, enabling them to exhibit better memory performance than low-performers at test. While such a strategy could provide more effective encoding fostering clearer subsequent representations, it is noteworthy that even high-performers in the present study perform at levels clearly below those of young participants in an identical experiment (see Wiese, 2012). Accordingly, even high-performers may not be able to fully compensate for age-related decline in face memory.

The present study is, to our knowledge, the first to examine ERP correlates of the ORB in older adult participants. The finding of an ORB independent of overall performance indicates that the fine-tuning of the face processing system toward faces of particular expertise is preserved in older adults. In line with this interpretation, the specific pattern of N170 ethnicity effects was found to parallel the behavioral ORB. In addition, a more bilateral N170 response in high-performing older adults suggests a partial compensation for general age-related decline in face perception by recruiting additional neural resources in the left hemisphere. In conclusion, the present results indicate that older adults' face processing system, even when working less efficiently, may still exhibit preserved expertise-related specialization toward own-race faces.