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Gender differences in memory processing: Evidence from event-related potentials to faces
Brain and Cognition 57 (2005) 84–92 www.elsevier.com/locate/b&c
Gender differences in memory processing: Evidence from event-related potentials to faces Franc¸ois Guillem*, Melodee Mograss Centre de Recherche F-Seguin, Hoˆpital L-H Lafontaine, 7331, rue Hochelaga, Montreal, Que., Canada H1N 3V2 Accepted 12 August 2004
Abstract This study investigated gender differences on memory processing using event-related potentials (ERPs). Behavioral data and ERPs were recorded in 16 males and 10 females during a recognition memory task for faces. The behavioral data results showed that females performed better than males. Gender differences on ERPs were evidenced over anterior locations and involve the modulation of two spatially and temporally distinct components. These results are in general accordance with the view that males and females differ in the cognitive strategies they use to process information. Specifically, they could differ in their abilities to maintain information over interference and in the processing of the intrinsic contextual attributes of items, respectively, associated with the modulation of two anterior components. These interpretations lend support to the view that processing in females entails more detailed elaboration of information content than in males. Processing in males is more likely driven by schemas or overall information theme. 2004 Elsevier Inc. All rights reserved.
1. Introduction Since the landmark study of Maccoby and Jacklin (1974), numerous studies have been interested in human gender differences in cognition and its cerebral basis. The most robust finding is that females perform relatively better on tasks involving production, comprehension, fine motor skills, and perceptual speed; whereas, males perform better on tasks involving visuospatial operations and fluid reasoning (Beatty, 1984; Halpern, 1997; Levy & Heller, 1992). Consistently, females also perform better on episodic memory tasks including delayed recall and recognition than do males, but males and females do not differ on working, immediate and semantic memory tasks (Halpern, 2000; Herlitz, Nilsson, & Backman, 1997; Herlitz, Airaksinen, & Nordstrom, 1999; Silverman & Eals, 1992; Wilson & Vandenberg, 1978). Since mnemonic capacity per se does not differ *
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0278-2626/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2004.08.026
between males and females (Maccoby & Jacklin, 1974), it has been proposed that the gender differences in memory performance reflect underlying differences in the strategies used to process information (McGivern et al., 1997; Meyers-Levy, 1989). Female processing entails more detailed elaboration of information content than males. In contrast, male processing is more likely to be driven by schemas or overall information theme (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). Most research in this area assumes that gender differences in cognitive strategies reflect differences in the functional organization of the brain. In general, neuropsychological observations suggest that anterior lesions cause greater deficits in females than in males (Kimura, 1983; Kimura, 1987; Kimura & Harshman, 1984); however, antero-posterior differences between genders, have not been replicated in other studies (De Renzie, Faglioni, & Fenari, 1980; Kertesz & Sheppard, 1981). On the other hand, some studies reported that left sided vascular lesions (McGlone, 1977, 1978) or lesions restricted
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to the left temporal lobe (Smith & Milner, 1984) produce more severe memory impairment in males than in females. Gender differences in cerebral asymmetry received support from morphometric studies showing a greater leftward asymmetry in males than in females (Good et al., 2001; Yucel et al., 2001). Other studies reported no overall difference or differential patterns of asymmetry for localized brain regions (Foundas, Faulhaber, Kulynych, Browning, & Weinberger, 1999; Nopoulos, Flaum, OÕLeary, & Andreasen, 2000). Furthermore, it has been proposed that the apparent gender difference in hemispheric asymmetry could result from a difference in interhemispheric connectivity and it is now a rather ÔclassicÕ view that females have less marked asymmetry due to larger splenium than males (Davatzikos & Resnick, 1998; Dorion et al., 2000; Oka et al., 1999), even though various studies did not replicate the results (Bishop & Wahlsten, 1997; Constant & Ruther, 1996). Finally, little morphological support is found for behavioral differences related to gender and if any, they seem to be subtle and superimposed on a high interindividual variability. In fact, the more recent advances in brain imaging methods suggest that gender differences are more likely related to a functional dimorphism at the cytoarchitectural level. Some studies found higher neuronal densities and neuronal number in men than women, and a reciprocal increase in neuropil volumes in females than in males (De Courten-Myers, 1999; Rabinowicz et al., 2002). This neuronal dimorphism implies differences in neuronal activity and connectivity that could provide a better account for the gender difference in cognitive strategies than the general anatomical views. One mean of investigating the cognitive functioning of the brain is the use of event-related potentials (ERPs). This method provide electrophysiological indices directly related to the neural and synaptic activities and permit a chronometric analysis of the discrete processes involved in the treatment of information, as well as reasonable inferences on the localization of brain areas that appear differentially involved (Picton, Lins, & Scherg, 1995). Some studies investigating gender differences with ERPs have reported larger component (P300) amplitudes in females than in males (Desrocher, Smith, & Taylor, 1995; Hoffman & Polish, 1999; Polich & Martin, 1992). Assuming that ERPs are generated by the local extracellular current flows that result from the synchronous activation of synapses, the observed amplitude difference between genders is consistent with the larger neuropil volumes in females. Other studies found a reverse gender differences, larger ERP amplitudes being observed in males. However, this observation seems to depend on other interacting factors. First, there is a gender difference in the scalp distribution of ERPs (Golgeli et al., 1999; Hantz, Marvin, Kreilick, & Chapman, 1996). Females show a larger antero-posterior amplitude
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gradient than males that is consistent with lesion studies suggesting that the anterior part of the brain plays a more critical role in females. Second, the gender difference on ERPs are influenced by the emotional valence (e.g., expression or attractiveness) of the stimuli (Oliver-Rodriguez, Guan, & Johnston, 1999; Orozco & Ehlers, 1998) and, in females, this effect appears to interact with the menstrual phase (Krug, Plihal, Fehm, & Born, 2000; Oliver-Rodriguez et al., 1999). In fact, no effect of menstrual phase on P300 is obtained with affectively neutral stimuli (Fleck & Polich, 1988), whereas phase difference appears when emotional stimuli were used (Johnston & Wang, 1991). For the most part, these studies used simple discrimination tasks that are unlikely to capture adequately the strategic processes thought to differentiate between the two genders. Given the relative consistency of the gender difference in episodic memory, an ERP task featuring memory could be more appropriate. In fact, two studies have used such a design. The first (Taylor, Smith, & Iron, 1990) contrasted male and female participants on ERPs recorded in verbal and non-verbal recognition memory tasks. The results showed that females displayed larger positive amplitude over anterior locations than males in the non-verbal task, whereas males displayed more positive ERPs over posterior locations in the verbal task. In another study comparing prepubertal males and females participating in a face recognition task, a rightward hemispheric asymmetry in males and a leftward asymmetry in females was found (Everhart, Shucard, Quatrin, & Shucard, 2001). Of interest is that these studies propose an anatomo-functional account of the gender difference both along the antero-posterior and left–right dimensions that are consistent with the literature in the field. Nevertheless, they have not used the full capability that is now offered by the ERPs recorded in recognition memory tasks. In recognition memory tasks, the basic finding is that the ERP elicited by the first presentation of an item (i.e., new item) are relatively less positive than those elicited by the second presentation of the same item (i.e., old stimuli) (Halgren, 1990; Rugg & Doyle, 1994). This modulation, usually referred to as the ÔERP old/new effect,Õ is elicited for various types of stimuli (i.e., words, pictures or faces) and in a wide variety of tasks (i.e., explicit or implicit tasks). In fact, it has been found that the ERP old/new effect is not a unitary phenomenon. Numerous studies have shown that the ERP old/new effect develops approximately 250 ms post-stimulus and lasts for a duration of 800 ms. It is composed of a series of ÔeffectsÕ distinguished by their task correlates, timing, and scalp topography, each reflecting the contribution of a discrete cognitive process to memory performance (Guillem, Bicu, & Debruille, 2001a; Johnson, Kreiter, Russo, & Zhu, 1998; Rugg et al., 1998). The main contribution to the ERP old/new effect is provided by
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the modulation of two posteriorly distributed components. The first is a negative component elicited within 300–500 ms, termed N400 and the second is a positive wave elicited within 400–800 ms termed P600. These components, respectively, reflect the integration of the information provided by the stimulus with personal knowledge (Holcomb, 1993; Rugg & Doyle, 1994) and the mnemonic binding processes that links the different aspects of information into a coherent representation (Guillem et al., 2001a; VanPetten, Kutas, Kluender, Mitchiner, & McIsaac, 1991). More recently, the additional contribution of at least two anteriorly distributed effects spanning the N400–P600 latency range has been evidenced. Interestingly, these effects are more related to processing strategies. An early and long lasting Ôfronto-polar effectÕ has been related to the selection and maintenance of items in the face stimuli of interfering information (Guillem et al., 2001a) and a later Ôfrontocentral effectÕ (sometimes with a right predominance) elicited between 300 and 500 ms is thought to reflect monitoring processes (Allan, Wilding, & Rugg, 1998) or more specifically the integration of the intrinsic context (Guillem et al., 2001a). This study was designed to define more precisely which discrete cognitive processes are involved in gender difference on memory performance. To this end, ERPs were recorded during a continuous recognition memory task for unfamiliar faces. This task shares its design with TaylorÕs study (Taylor et al., 1990) and its stimulus type with the EverhartÕs one (Everhart et al., 2001), i.e., with the two reports that demonstrated gender difference in memory processing. In addition, previous studies have shown that this protocol permits dissociation of the above mentioned contributors to the ERP old/new effect.
2. Methods 2.1. Participants Sixteen males and ten females right-handed volunteers participated in the experiment. Their ages ranged from 20 to 35 years (males: 27.6 ± 5.5; females: 24.7 ± 3.6) and they had completed at least 10 years of education (males: 15.9 ± 4.0; females: 17.4 ± 2.1). Their levels of education, as well as those of their parents were rated on a 5-point scale: 1, Primary school; 2, Secondary school; 3, Bachelor; 4, Master or equivalent; and 5, Ph.D. (males: Ss 3.6 ± 1.5, parents 2.8 ± 1.4; females: Ss 3.7 ± 0.7, parents 3.1 ± 1.8). All participants had normal or corrected to normal vision and reported free of any current or past neurological or psychiatric disease. These socio-demographic data were collected during an interview after the subjects were fully informed of the protocol and signed a consent form. None was familiar with the experimental design of the study.
2.2. Stimuli Stimuli consisted of 438 color photographs representing personsÕ faces unknown to the subjects. These stimuli were taken from the MED bank of face (Debruille, Pelchat, Dubuc, & Brodeur, 1997) that is composed of front view color photographs of faces taken in the same conditions (background and light). Although the photographed persons were asked to keep the most neutral expression, other persons subsequently rated each face as friendly, unfriendly or neutral. To minimize the possible confounding effects of emotional expression, the faces chosen as stimuli for this experiment were first those with the higher neutral scores and the set was completed with friendly and unfriendly faces in the same proportion. The whole set was then divided into three sub-sets counterbalanced for expression and gender. The sub-sets were used to construct three blocks of 146 stimuli placed pseudo-randomly in a continuous repetition task sequence. In each block, 73 faces occurred a first time (new items) and reappeared subsequently after 2–20 intervening items (repeated items). 2.3. Procedure Subjects sat in a comfortable chair in a sound-attenuated room and were told to stare at a fixation cross placed at the center of a computer screen. Faces were presented on a gray background at the center of this screen 1.5 m away from the subjects sustaining a visual angle of 5. Each face remained for 500 ms and was replaced by gray screen for 2.5–3.5 s. To reduce the occurrence of blinks during stimulus presentation, the word ÔblinkÕ then appeared for 630 ms and was replaced by gray for 2.5–3.5 s. The fixation cross was always present except during the presentations of the faces and of the word Ôblink.Õ The test begun after a practice session using faces not included in the test blocks. Subjects were required to indicate for each stimulus, whether it has been previously presented (old items) or not (new items) by pressing arrow keys on a computer keyboard. Subjects had 3–5 min resting pauses between each block to prevent fatigue. The reaction time and ERP data reported correspond to trials associated with correct response only. 2.4. ERP recording and analysis The EEG was recorded from 13 electrodes placed according to the International 10–20 System. Midline recording sites (Fz, Cz, and Pz) were used, along with lateral electrode pairs over anterior frontal (Fp1, Fp2), fronto-temporal (F7, F8), parietal (P3, P4), anterior temporal (T3, T4), and posterior temporal (T5, T6) sites. An additional active electrode was placed on the left earlobe (A1). Vertical and horizontal eye movements and
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blinks were monitored via electrodes placed below the left eye and on the outer canthus of this eye, respectively. All channels were referenced to the right earlobe (A2) during recording and re-referenced offline to linked earlobes. An electrode placed at Fpz served as the ground. Impedance of all electrodes was maintained below 5 kX. EEG was recorded continuously with a bandpass of 0.01–30 Hz, digitized on-line at a rate of 250 Hz, and stored along with the codes identifying the stimulus type, the stimulus onset and the subjectÕs responses. Offline averaging were performed after EOG correction using statistical software algorithms and after rejection of epoch with amplifier blocking exceeding 100 ms. For both direct and indirect tests, ERPs were computed from 0 to 1000 ms post-onset with a 200 ms pre-stimulus baseline for new items and old (i.e., already presented) items. ERP peaks were identified by visual inspection of the individual traces recorded at Cz within the 200–800 ms post-onset. This latency window was selected as typical for previous studies of ERP old/new effect. Amplitudes were quantified with respect to the baseline within several time windows. For each peak, the lower limit of the time window was defined as the median latency between the current and the previous peak. The upper limit corresponded to the median latency between the current and the following peak. This procedure resulted in non-overlapping time window of varying duration that allow to capture amplitude effects separately for each peak (Guillem et al., 2001a). As in our previous studies, the first peak was a negative deflection peaking at 246 ms post-stimulus; the N300, which was analyzed in a 201–315 ms time window. The other peaks were a P400, (315–410 ms), a N500 (410–526 ms) and a P700 (526–714 ms). 2.5. Data analysis Potential differences between patients groups (female · male) on socio-demographic data were assessed using univariate ANOVAs. Reaction times (RTs) were compared using ANOVAs with ÔgroupÕ (female and male) as between-subjects factor and ÔconditionÕ (old and new) as within-subject variable. Scores (% hits and % false alarms) and a discrimination index (d 0 ) were analyzed using univariate ANOVAs with group as a between-subjects factor. ERP data were analyzed separately for midline and lateral sites using mixed-model ANOVAs. For the midline sites, the model included the ÔgroupÕ (female · male) as a between subject factor and the ÔconditionÕ (old · new) and electrode ÔsiteÕ (Fz, Cz, and Pz) as within-subject variables. For the lateral sites, the model included the ÔgroupÕ (female · male) as a between subject factor and the ÔconditionÕ (old · new), the ÔregionÕ (fronto-polar: Fp1, Fp2; fronto-lateral: F7, F8; anterior temporal:
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T3, T4; posterior temporal: T5, T6; parietal: P3, P4) and ÔlateralityÕ (left, right) as within-subject variables. In all analyses, degrees of freedom were adjusted using the Geisser-Greenhouse procedure where appropriate (uncorrected df are reported with the epsilon, e values and corrected p values). Differences in scalp distribution across conditions were also analyzed after normalization of the data (McCarthy & Wood, 1985). This procedure allows one to account for the possibility that a given scalp distribution effect can be due to multiplicative differences in distinct neural source strength. Thus, interactions involving the factor of site were usually reported if significant in the scaled data set (Swick & Knight, 1997).
3. Results The comparison between the two groups showed no differences on socio-demographic data (all Fs < 2.21; all ps > .15). The ANOVA on recognition scores (%hits) revealed that females perform better than males (F(1,24) = 9.79; p = .005). They also tend to make fewer false alarms (F(1,24) = 3.58; p = .07). The analysis also showed that females better discriminate old from new items as reflected their higher d 0 index compared to males (F(1,24) = 9.02; p = .006). ANOVAs on RT data showed a significant effect of condition (F(1,24) = 19.89; p < .001) but no significant effect of group and interaction between the two factors, although females showed a somewhat greater facilitation (i.e., larger repetition effect) than in males (Table 1). The grand average waveforms presented in Fig. 1 show four main peaks similar to those previously reported in the same task (Guillem et al., 2001a). The ANOVA on midline data for the N300 resulted in significant effects of condition (F(1,24) = 7.32; p = .01) and site (F(2,48) = 24.09; p < .001; e = 0.664), with no effect or interaction involving the factors of condition and group. The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 10.54; p = .003) and site (F(4,96) = 13.17; p < .001; e = 0.351) with no other effect or interaction involving the factors of condition, laterality and group. These results indicate that ERP
Table 1 Behavioral results (SD in parentheses) Males
Females
Reaction time for correct responses (ms) New 1036.3 (247.1) Old 940.6 (218.2)
940.9 (161.4) 796.6 (105.9)
Scores % Hits % False alarms
84.4 (8.9) 12.6 (9.5)
93.7 (3.5) 6.6 (4.1)
d0
1.9 (0.6)
2.8 (0.9)
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Fig. 1. Grand averaged ERPs obtained from the midline electrode sites (Fz, Cz, and Pz) in males and females for correctly identified new items (thin lines) and correctly recognized old items (thick lines).
within the N300 time window are similarly modulated by repetition in males and females. The ANOVA on midline data for the P400 resulted in significant effects of condition (F(1,24) = 25.07; p < .001) and site (F(2,48) = 32.47; p < .001; e = 0.642). There was also a trend for a significant effect of group (F(1,24) = 3.09; p = .09) but no interaction between factors. The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 37.86; p < .001), site (F(4,96) = 31.22; p < .001; e = 0.384) and laterality (F(1,24) = 8.76; p = .007). As for the midline data, there was a trend for a significant effect of group (F(1,24) = 3.02; p = .09). As shown in Fig. 1, these results reflect that ERP amplitude is generally larger in females than in males, whereas the ERP old/new effect is similar across gender. Noteworthy, interactions between condition, site and group were present for both the midline (F(2,48) = 3.5; p = .05; e = 0.716) and lateral analyses (F(4,96) = 6.06; p = .01; e = 0.340), but they were not confirmed on scaled data. These observations suggest that gender difference in the topography of ERP old/ new effect starts within this time window. The Fig. 2 showed that the difference is larger over fronto-polar sites (Fp1, Fp2) and particularly over the right hemisphere. This could account for the observed laterality effect. The ANOVA on the midline data obtained in the N400 time window showed a significant effects of condition (F(1,24) = 70.85; p < .001), sites (F(2,48) = 34.49; p < .001; e = 0.628), and group (F(1,24) = 5.45; p = .03). There were also significant interactions between condition and group (F(1,24) = 9.31; p = .005), condition and site (F(2,48) = 5.93; p = .012; e = 0.715), and between the three factors (F(2,48) = 6.54; p = .008; e = 0.715). These results indicate that males and females differ in their the topography of their ERP old/new effect.
The Fig. 2 shows that that females displayed a larger effect than males over fronto-central sites (Fz, Cz). The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 114.51; p < .001), site (F(4,96) = 29.22; p < .001; e = 0.369), laterality (F(1,24) = 4.98; p = .04), and group (F(1,24) = 6.00; p = .02). There were also significant interactions between condition and group (F(1,24) = 13.96; p = .001), condition and site (F(4,96) = 11,00; p < .001; e = 0.395), between condition, site, and group (F(4,96) = 4.84; p = .02; e = 0.395), and between condition, laterality, and group (F(1,24) = 4.19; p = .05). Again, these results indicate a differential topography of the ERP old/new effect across genders. The Fig. 2 showed that the interactions reflect the larger effect in females at fronto-polar sites (Fp1, Fp2), particularly over the right hemisphere and the grossly similar effect over posterior sites. The ANOVA on the midline data obtained in the P600 time window showed a significant effect of condition (F(1,24) = 16.78; p < .001), sites (F(2,48) = 40.79; p < .001; e = 0.642), and group (F(1,24) = 8.80; p = .007). There were also a significant interactions between condition and group (F(1,24) = 45.60; p = .04). The Fig. 2 showed that these results reflect the generally larger ERP old/new effect in females. As in the N400 time window, the difference is more evident over fronto-central sites (Fz, Cz). The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 28.941; p < .001), site (F(4,96) = 2425; p < .001; e = 0.369), group (F(1,24) = 9.88; p = .004), and a marginally significant effect of laterality (F(1,24) = 3.87; p = .06). There were significant interactions between condition and group (F(1,24) = 5.66; p = .03) and between condition, site, and laterality (F(4,96) = 9.83; p < .001; e = 0.483). Although not confirmed on scaled data, there were also
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Fig. 2. Scalp distribution of the ERP old/new effect (old minus new amplitude difference) obtained in males and females expressed in raw data in lV (left panel) and normalized data (right panel).
a significant condition · site (F(4,96) = 3.38; p < .05; e = 0.395) interaction and a trend for a condition · site · laterality · group interaction (F(4,96) = 2.49; p = .09; e = 0.483). Generally, these results indicate that the ERP old/new effect within the P600 time window is similar across genders. Nevertheless, both the additional interactions and the Fig. 2 suggest a tendency for the ERP old/new effect to be larger over right fronto-polar sites in females, as observed in the N400 time window.
4. Discussion The results on the behavioral data show that, although there is no major difference in recognition latency, between the two gender groups, females have a higher hit rate and lower false alarm rate than males. This observation replicates the general finding from the literature on gender difference in memory processing
(Herlitz et al., 1997; Herlitz et al., 1999; Ragland, Coleman, Gur, Glahn, & Gur, 2000; Silverman & Eals, 1992; Wilson & Vandenberg, 1978). In fact such a difference is observed consistently on recall and recognition tasks featuring episodic processes, such as those required for the effective processing of unfamiliar faces used here but not on working, immediate, and semantic memory tasks. In addition, the present results show the lower performance of males is mainly due to their larger number of miss responses, which suggests that they maintain less information or that they form more labile representation than females (see also Waters & Schreiber, 1991). They also tend to make more false alarms, which may indicate that the representations formed are less specific, i.e., more sensitive to subjective familiarity (see Schacter, Norman, & Koutstaal, 1998) and interference (see Kramer, Delis, Kaplan, OÕDonnell, & Prifitera, 1997; Palmer & Folds-Bennett, 1998), than in females. This interpretation is consistent with the view that females
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engage in more detailed elaboration of information that lead to more specific and less labile representation, whereas males rely on less elaborated schemas or overall information theme (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). The results of the ERP analysis show generally larger amplitudes in females than in males. This difference, present as early as the N300 and lasts until the P600, is particularly evident anteriorly (Fig. 1). This observation is comparable with that of Taylor (Taylor et al., 1990) on ERPs recorded in a non-verbal memory task, as well as with the results of some studies using simple discrimination tasks (Desrocher et al., 1995; Hoffman & Polish, 1999; Polich & Martin, 1992). As already mentioned in Section 1, the gender difference in ERP amplitudes could be related to differences in neuropil volumes (i.e., larger in females) (De Courten-Myers, 1999; Rabinowicz et al., 2002). However, neuropil difference is present in the whole brain and thus, it cannot account for the relative localization (anterior vs. posterior) and its material specificity (verbal vs. non-verbal) reported by Taylor (Taylor et al., 1990). One possibility is that the cytoarchitectural difference is better expressed in some brain regions more specifically recruited to perform in particular (experimental) conditions. In other words, task or material specific functional differences in information processing may overlap the neuroanatomical differences. This is likely to be the case since our results evidence more subtle gender differences in the modulation of the ERPs, i.e., in the old/new effect. Some spatially and temporally localized effects contributing to the general ERP old/new effects (see Section 1) display gender differences, whereas others do not. No gender difference in the ERP old/new effect is observed over posterior sites in the N400 time window. If one accepts the classical interpretation that the posterior N400 is modulated by the ease with which the incoming information is integrated with personal knowledge (i.e., the more the positive the amplitude, the easier the integration) (Holcomb, 1993; Rugg & Doyle, 1994), this result indicates that males and females perform this process as efficiently. This is in fact reminiscent with the lack of gender difference on semantic memory and priming tasks reported in behavioral studies (Herlitz et al., 1997). However, Taylor (Taylor et al., 1990) showed that in a similar task using verbal stimuli, males produced more positive ERPs over posterior sites during the N400 than females. These discrepancies are likely related to the use of different materials. Following the above interpretation of the N400, TaylorÕs results could reflect that males are more efficient than females at integrating information already represented in semantic memory, such as words. This interpretation is consistent with the view that male processing is driven mainly by preexisting schemas (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). If so, no difference
should have been expected at the knowledge integration stage (i.e., N400) for stimuli that have no pre-established specific representation (except in the form of a general face schema) such as the unfamiliar faces used here. The results also show no gender difference in the ERP old/new effect on posterior P600 data. According to the classical interpretation of the P600 (Guillem et al., 2001a; VanPetten et al., 1991), this observation indicates that males and females are similarly able to bind the different aspects of information into a coherent representation. Thus, how can the differences observed on behavioral performances be accounted for? A plausible explanation is that the group differences do not differ quantitatively in the amount of information bound or retrieved as reflected in the P600 old/new effect, but in the quality of the binding that makes the representations retrievable as reflected in behavioral scores (see Guillem et al., 2001b; Guillem et al., 2003, for a similar view). As argued above, males may form more labile and less specific representations than females. In fact, if the P600 reflects the endpoint where the information extracted from the stimulus converged, the qualitative difference between genders is likely to rely on differences at antecedent processing stages those reflected in earlier ERP components. This is supported by the gender differences observed on the earlier contributors of the ERP old/new effect distributed over anterior sites. More specifically, a long-lasting gender difference is observed over fronto-polar sites from the P400 to the P600 time windows and it is likely predominating within the P400–N400 latency range as shown on normalized data (Fig. 2). This fronto-polar contributor of the ERP old/new effect has been previously related to the selection and maintenance of items in the face of interfering information (Guillem et al., 2001a). By this view, the lower effect in males indicates that they require a similar amount of interference inhibition to process old and new items. Conversely, the large effect in females indicates a facilitated processing of old items. This interpretation is consistent with the behavioral data concerning false alarms that suggested the greater interference sensitivity of males in relation with their preferential schematic or global processing of information. It is also of note that the gender difference on the fronto-polar effect is somewhat weak, as it is the case for the difference on false alarms rate. A more reliable gender difference is evidenced over fronto-central sites during the N400–P600 latency range. Interestingly, this effect is generally associated with strategic monitoring processes (Allan et al., 1998). More specifically, it could represent the processing of the intrinsic contextual attributes of items. This process is particularly critical for complex and unfamiliar stimuli that require the formation of representations that are sufficiently distinctive to be retrieved subsequently (Guillem et al., 2001a). The larger fronto-central old/
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new effect observed in females is thus, in well accordance with the view that they entail more detailed elaboration of information than males. In summary, the results of the present study obtained with ERP measures remarkably corroborate the behavioral and neuroanatomical literature concerning gender differences in memory processing. Generally, they are consistent with the idea that males and females differ in the cognitive strategies they use to process information. In addition, ERPs provide a more dynamic account in which gender differences in memory performance rely more particularly on specific stages occurring in the cascade of the cognitive and neural mechanisms involved in memory processing.
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Rabinowicz, T., Petetot, J. M., Gartside, P. S., Sheyn, D., Sheyn, T., & de Courten-Myers, G. M. (2002). Structure of the cerebral cortex in men and women. Journal of Neuropathology and Experimental Neurology, 61, 46–57. Ragland, J. D., Coleman, A. R., Gur, R. C., Glahn, D. C., & Gur, R. E. (2000). Sex differences in brain-behavior relationships between verbal episodic memory and resting regional cerebral blood flow. Neuropsychologia, 38, 451–461. Rugg, M. D., & Doyle, M. C. (1994). Event-related potentials and stimulus repetition in direct and indirect tests of memory. In H. J. Heinze, T. F. Mu¨nte, & G. R. Mangun (Eds.), Cognitive electrophysiology (pp. 124–148). Boston: Birkha¨user. Rugg, M. D., Mark, R. E., Walla, P., Schloerscheidt, A. M., Birch, C. S., & Allan, K. (1998). Dissociation of the neural correlates of implicit and explicit memory. Nature, 392, 595–598. Schacter, D. L., Norman, K. A., & Koutstaal, W. (1998). The cognitive neuroscience of constructive memory. Annual Review of Psychology, 49, 289–318. Silverman, R., & Eals, M. (1992). Sex differences in spatial abilities: Evolutionary theory and data. In J. H. Barkow, L. Cosmides, & J. Tooby (Eds.), The adapted mind: evolutionary psychology and the generation of culture. New York: Oxford University Press. Smith, M., & Milner, B. (1984). Residual memory deficits after unilateral cerebral excision. Paper read at the Annual Meeting of the International Neuropsychology Symposium, Beaune, France. Swick, D., & Knight, R. T. (1997). Event-related potentials differentiate the effects of aging on word and nonword repetition in explicit and implicit memory tasks. Journal of Experimental Psychology: Learning Memory & Cognition, 23, 123–142. Taylor, M. J., Smith, M. L., & Iron, K. S. (1990). Event-related potential evidence of sex differences in verbal and nonverbal memory tasks. Neuropsychologia, 28, 691–705. VanPetten, C., Kutas, M., Kluender, R., Mitchiner, M., & McIsaac, H. (1991). Fractionating the word repetition effect with eventrelated potentials. Journal of Cognitive Neuroscience, 3, 131–150. Waters, H. S., & Schreiber, L. L. (1991). Sex differences in elaborative strategies: A developmental analysis. Journal of Experimental Child Psychology, 52, 319–335. Wilson, J. R., & Vandenberg, S. G. (1978). Sex differences in cognition: Evidence from the Hawaii family study. In T. E. McGill, D. A. Dewsbury, & B. D. Sachs (Eds.), Sex and behavior: Status and prospectus. New York: Plenum Press. Yucel, M., Stuart, G. W., Maruff, P., Velakoulis, D., Crowe, S. F., Savage, G., et al. (2001). Hemispheric and gender-related differences in the gross morphology of the anterior cingulate/paracingulate cortex in normal volunteers: An MRI morphometric study. Cerebral Cortex, 11, 17–25.
Gender differences in memory processing: Evidence from event-related potentials to faces Franc¸ois Guillem*, Melodee Mograss Centre de Recherche F-Seguin, Hoˆpital L-H Lafontaine, 7331, rue Hochelaga, Montreal, Que., Canada H1N 3V2 Accepted 12 August 2004
Abstract This study investigated gender differences on memory processing using event-related potentials (ERPs). Behavioral data and ERPs were recorded in 16 males and 10 females during a recognition memory task for faces. The behavioral data results showed that females performed better than males. Gender differences on ERPs were evidenced over anterior locations and involve the modulation of two spatially and temporally distinct components. These results are in general accordance with the view that males and females differ in the cognitive strategies they use to process information. Specifically, they could differ in their abilities to maintain information over interference and in the processing of the intrinsic contextual attributes of items, respectively, associated with the modulation of two anterior components. These interpretations lend support to the view that processing in females entails more detailed elaboration of information content than in males. Processing in males is more likely driven by schemas or overall information theme. 2004 Elsevier Inc. All rights reserved.
1. Introduction Since the landmark study of Maccoby and Jacklin (1974), numerous studies have been interested in human gender differences in cognition and its cerebral basis. The most robust finding is that females perform relatively better on tasks involving production, comprehension, fine motor skills, and perceptual speed; whereas, males perform better on tasks involving visuospatial operations and fluid reasoning (Beatty, 1984; Halpern, 1997; Levy & Heller, 1992). Consistently, females also perform better on episodic memory tasks including delayed recall and recognition than do males, but males and females do not differ on working, immediate and semantic memory tasks (Halpern, 2000; Herlitz, Nilsson, & Backman, 1997; Herlitz, Airaksinen, & Nordstrom, 1999; Silverman & Eals, 1992; Wilson & Vandenberg, 1978). Since mnemonic capacity per se does not differ *
Corresponding author. Fax: +1 514 251 2617. E-mail address: [email protected] (F. Guillem).
0278-2626/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2004.08.026
between males and females (Maccoby & Jacklin, 1974), it has been proposed that the gender differences in memory performance reflect underlying differences in the strategies used to process information (McGivern et al., 1997; Meyers-Levy, 1989). Female processing entails more detailed elaboration of information content than males. In contrast, male processing is more likely to be driven by schemas or overall information theme (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). Most research in this area assumes that gender differences in cognitive strategies reflect differences in the functional organization of the brain. In general, neuropsychological observations suggest that anterior lesions cause greater deficits in females than in males (Kimura, 1983; Kimura, 1987; Kimura & Harshman, 1984); however, antero-posterior differences between genders, have not been replicated in other studies (De Renzie, Faglioni, & Fenari, 1980; Kertesz & Sheppard, 1981). On the other hand, some studies reported that left sided vascular lesions (McGlone, 1977, 1978) or lesions restricted
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to the left temporal lobe (Smith & Milner, 1984) produce more severe memory impairment in males than in females. Gender differences in cerebral asymmetry received support from morphometric studies showing a greater leftward asymmetry in males than in females (Good et al., 2001; Yucel et al., 2001). Other studies reported no overall difference or differential patterns of asymmetry for localized brain regions (Foundas, Faulhaber, Kulynych, Browning, & Weinberger, 1999; Nopoulos, Flaum, OÕLeary, & Andreasen, 2000). Furthermore, it has been proposed that the apparent gender difference in hemispheric asymmetry could result from a difference in interhemispheric connectivity and it is now a rather ÔclassicÕ view that females have less marked asymmetry due to larger splenium than males (Davatzikos & Resnick, 1998; Dorion et al., 2000; Oka et al., 1999), even though various studies did not replicate the results (Bishop & Wahlsten, 1997; Constant & Ruther, 1996). Finally, little morphological support is found for behavioral differences related to gender and if any, they seem to be subtle and superimposed on a high interindividual variability. In fact, the more recent advances in brain imaging methods suggest that gender differences are more likely related to a functional dimorphism at the cytoarchitectural level. Some studies found higher neuronal densities and neuronal number in men than women, and a reciprocal increase in neuropil volumes in females than in males (De Courten-Myers, 1999; Rabinowicz et al., 2002). This neuronal dimorphism implies differences in neuronal activity and connectivity that could provide a better account for the gender difference in cognitive strategies than the general anatomical views. One mean of investigating the cognitive functioning of the brain is the use of event-related potentials (ERPs). This method provide electrophysiological indices directly related to the neural and synaptic activities and permit a chronometric analysis of the discrete processes involved in the treatment of information, as well as reasonable inferences on the localization of brain areas that appear differentially involved (Picton, Lins, & Scherg, 1995). Some studies investigating gender differences with ERPs have reported larger component (P300) amplitudes in females than in males (Desrocher, Smith, & Taylor, 1995; Hoffman & Polish, 1999; Polich & Martin, 1992). Assuming that ERPs are generated by the local extracellular current flows that result from the synchronous activation of synapses, the observed amplitude difference between genders is consistent with the larger neuropil volumes in females. Other studies found a reverse gender differences, larger ERP amplitudes being observed in males. However, this observation seems to depend on other interacting factors. First, there is a gender difference in the scalp distribution of ERPs (Golgeli et al., 1999; Hantz, Marvin, Kreilick, & Chapman, 1996). Females show a larger antero-posterior amplitude
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gradient than males that is consistent with lesion studies suggesting that the anterior part of the brain plays a more critical role in females. Second, the gender difference on ERPs are influenced by the emotional valence (e.g., expression or attractiveness) of the stimuli (Oliver-Rodriguez, Guan, & Johnston, 1999; Orozco & Ehlers, 1998) and, in females, this effect appears to interact with the menstrual phase (Krug, Plihal, Fehm, & Born, 2000; Oliver-Rodriguez et al., 1999). In fact, no effect of menstrual phase on P300 is obtained with affectively neutral stimuli (Fleck & Polich, 1988), whereas phase difference appears when emotional stimuli were used (Johnston & Wang, 1991). For the most part, these studies used simple discrimination tasks that are unlikely to capture adequately the strategic processes thought to differentiate between the two genders. Given the relative consistency of the gender difference in episodic memory, an ERP task featuring memory could be more appropriate. In fact, two studies have used such a design. The first (Taylor, Smith, & Iron, 1990) contrasted male and female participants on ERPs recorded in verbal and non-verbal recognition memory tasks. The results showed that females displayed larger positive amplitude over anterior locations than males in the non-verbal task, whereas males displayed more positive ERPs over posterior locations in the verbal task. In another study comparing prepubertal males and females participating in a face recognition task, a rightward hemispheric asymmetry in males and a leftward asymmetry in females was found (Everhart, Shucard, Quatrin, & Shucard, 2001). Of interest is that these studies propose an anatomo-functional account of the gender difference both along the antero-posterior and left–right dimensions that are consistent with the literature in the field. Nevertheless, they have not used the full capability that is now offered by the ERPs recorded in recognition memory tasks. In recognition memory tasks, the basic finding is that the ERP elicited by the first presentation of an item (i.e., new item) are relatively less positive than those elicited by the second presentation of the same item (i.e., old stimuli) (Halgren, 1990; Rugg & Doyle, 1994). This modulation, usually referred to as the ÔERP old/new effect,Õ is elicited for various types of stimuli (i.e., words, pictures or faces) and in a wide variety of tasks (i.e., explicit or implicit tasks). In fact, it has been found that the ERP old/new effect is not a unitary phenomenon. Numerous studies have shown that the ERP old/new effect develops approximately 250 ms post-stimulus and lasts for a duration of 800 ms. It is composed of a series of ÔeffectsÕ distinguished by their task correlates, timing, and scalp topography, each reflecting the contribution of a discrete cognitive process to memory performance (Guillem, Bicu, & Debruille, 2001a; Johnson, Kreiter, Russo, & Zhu, 1998; Rugg et al., 1998). The main contribution to the ERP old/new effect is provided by
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the modulation of two posteriorly distributed components. The first is a negative component elicited within 300–500 ms, termed N400 and the second is a positive wave elicited within 400–800 ms termed P600. These components, respectively, reflect the integration of the information provided by the stimulus with personal knowledge (Holcomb, 1993; Rugg & Doyle, 1994) and the mnemonic binding processes that links the different aspects of information into a coherent representation (Guillem et al., 2001a; VanPetten, Kutas, Kluender, Mitchiner, & McIsaac, 1991). More recently, the additional contribution of at least two anteriorly distributed effects spanning the N400–P600 latency range has been evidenced. Interestingly, these effects are more related to processing strategies. An early and long lasting Ôfronto-polar effectÕ has been related to the selection and maintenance of items in the face stimuli of interfering information (Guillem et al., 2001a) and a later Ôfrontocentral effectÕ (sometimes with a right predominance) elicited between 300 and 500 ms is thought to reflect monitoring processes (Allan, Wilding, & Rugg, 1998) or more specifically the integration of the intrinsic context (Guillem et al., 2001a). This study was designed to define more precisely which discrete cognitive processes are involved in gender difference on memory performance. To this end, ERPs were recorded during a continuous recognition memory task for unfamiliar faces. This task shares its design with TaylorÕs study (Taylor et al., 1990) and its stimulus type with the EverhartÕs one (Everhart et al., 2001), i.e., with the two reports that demonstrated gender difference in memory processing. In addition, previous studies have shown that this protocol permits dissociation of the above mentioned contributors to the ERP old/new effect.
2. Methods 2.1. Participants Sixteen males and ten females right-handed volunteers participated in the experiment. Their ages ranged from 20 to 35 years (males: 27.6 ± 5.5; females: 24.7 ± 3.6) and they had completed at least 10 years of education (males: 15.9 ± 4.0; females: 17.4 ± 2.1). Their levels of education, as well as those of their parents were rated on a 5-point scale: 1, Primary school; 2, Secondary school; 3, Bachelor; 4, Master or equivalent; and 5, Ph.D. (males: Ss 3.6 ± 1.5, parents 2.8 ± 1.4; females: Ss 3.7 ± 0.7, parents 3.1 ± 1.8). All participants had normal or corrected to normal vision and reported free of any current or past neurological or psychiatric disease. These socio-demographic data were collected during an interview after the subjects were fully informed of the protocol and signed a consent form. None was familiar with the experimental design of the study.
2.2. Stimuli Stimuli consisted of 438 color photographs representing personsÕ faces unknown to the subjects. These stimuli were taken from the MED bank of face (Debruille, Pelchat, Dubuc, & Brodeur, 1997) that is composed of front view color photographs of faces taken in the same conditions (background and light). Although the photographed persons were asked to keep the most neutral expression, other persons subsequently rated each face as friendly, unfriendly or neutral. To minimize the possible confounding effects of emotional expression, the faces chosen as stimuli for this experiment were first those with the higher neutral scores and the set was completed with friendly and unfriendly faces in the same proportion. The whole set was then divided into three sub-sets counterbalanced for expression and gender. The sub-sets were used to construct three blocks of 146 stimuli placed pseudo-randomly in a continuous repetition task sequence. In each block, 73 faces occurred a first time (new items) and reappeared subsequently after 2–20 intervening items (repeated items). 2.3. Procedure Subjects sat in a comfortable chair in a sound-attenuated room and were told to stare at a fixation cross placed at the center of a computer screen. Faces were presented on a gray background at the center of this screen 1.5 m away from the subjects sustaining a visual angle of 5. Each face remained for 500 ms and was replaced by gray screen for 2.5–3.5 s. To reduce the occurrence of blinks during stimulus presentation, the word ÔblinkÕ then appeared for 630 ms and was replaced by gray for 2.5–3.5 s. The fixation cross was always present except during the presentations of the faces and of the word Ôblink.Õ The test begun after a practice session using faces not included in the test blocks. Subjects were required to indicate for each stimulus, whether it has been previously presented (old items) or not (new items) by pressing arrow keys on a computer keyboard. Subjects had 3–5 min resting pauses between each block to prevent fatigue. The reaction time and ERP data reported correspond to trials associated with correct response only. 2.4. ERP recording and analysis The EEG was recorded from 13 electrodes placed according to the International 10–20 System. Midline recording sites (Fz, Cz, and Pz) were used, along with lateral electrode pairs over anterior frontal (Fp1, Fp2), fronto-temporal (F7, F8), parietal (P3, P4), anterior temporal (T3, T4), and posterior temporal (T5, T6) sites. An additional active electrode was placed on the left earlobe (A1). Vertical and horizontal eye movements and
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blinks were monitored via electrodes placed below the left eye and on the outer canthus of this eye, respectively. All channels were referenced to the right earlobe (A2) during recording and re-referenced offline to linked earlobes. An electrode placed at Fpz served as the ground. Impedance of all electrodes was maintained below 5 kX. EEG was recorded continuously with a bandpass of 0.01–30 Hz, digitized on-line at a rate of 250 Hz, and stored along with the codes identifying the stimulus type, the stimulus onset and the subjectÕs responses. Offline averaging were performed after EOG correction using statistical software algorithms and after rejection of epoch with amplifier blocking exceeding 100 ms. For both direct and indirect tests, ERPs were computed from 0 to 1000 ms post-onset with a 200 ms pre-stimulus baseline for new items and old (i.e., already presented) items. ERP peaks were identified by visual inspection of the individual traces recorded at Cz within the 200–800 ms post-onset. This latency window was selected as typical for previous studies of ERP old/new effect. Amplitudes were quantified with respect to the baseline within several time windows. For each peak, the lower limit of the time window was defined as the median latency between the current and the previous peak. The upper limit corresponded to the median latency between the current and the following peak. This procedure resulted in non-overlapping time window of varying duration that allow to capture amplitude effects separately for each peak (Guillem et al., 2001a). As in our previous studies, the first peak was a negative deflection peaking at 246 ms post-stimulus; the N300, which was analyzed in a 201–315 ms time window. The other peaks were a P400, (315–410 ms), a N500 (410–526 ms) and a P700 (526–714 ms). 2.5. Data analysis Potential differences between patients groups (female · male) on socio-demographic data were assessed using univariate ANOVAs. Reaction times (RTs) were compared using ANOVAs with ÔgroupÕ (female and male) as between-subjects factor and ÔconditionÕ (old and new) as within-subject variable. Scores (% hits and % false alarms) and a discrimination index (d 0 ) were analyzed using univariate ANOVAs with group as a between-subjects factor. ERP data were analyzed separately for midline and lateral sites using mixed-model ANOVAs. For the midline sites, the model included the ÔgroupÕ (female · male) as a between subject factor and the ÔconditionÕ (old · new) and electrode ÔsiteÕ (Fz, Cz, and Pz) as within-subject variables. For the lateral sites, the model included the ÔgroupÕ (female · male) as a between subject factor and the ÔconditionÕ (old · new), the ÔregionÕ (fronto-polar: Fp1, Fp2; fronto-lateral: F7, F8; anterior temporal:
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T3, T4; posterior temporal: T5, T6; parietal: P3, P4) and ÔlateralityÕ (left, right) as within-subject variables. In all analyses, degrees of freedom were adjusted using the Geisser-Greenhouse procedure where appropriate (uncorrected df are reported with the epsilon, e values and corrected p values). Differences in scalp distribution across conditions were also analyzed after normalization of the data (McCarthy & Wood, 1985). This procedure allows one to account for the possibility that a given scalp distribution effect can be due to multiplicative differences in distinct neural source strength. Thus, interactions involving the factor of site were usually reported if significant in the scaled data set (Swick & Knight, 1997).
3. Results The comparison between the two groups showed no differences on socio-demographic data (all Fs < 2.21; all ps > .15). The ANOVA on recognition scores (%hits) revealed that females perform better than males (F(1,24) = 9.79; p = .005). They also tend to make fewer false alarms (F(1,24) = 3.58; p = .07). The analysis also showed that females better discriminate old from new items as reflected their higher d 0 index compared to males (F(1,24) = 9.02; p = .006). ANOVAs on RT data showed a significant effect of condition (F(1,24) = 19.89; p < .001) but no significant effect of group and interaction between the two factors, although females showed a somewhat greater facilitation (i.e., larger repetition effect) than in males (Table 1). The grand average waveforms presented in Fig. 1 show four main peaks similar to those previously reported in the same task (Guillem et al., 2001a). The ANOVA on midline data for the N300 resulted in significant effects of condition (F(1,24) = 7.32; p = .01) and site (F(2,48) = 24.09; p < .001; e = 0.664), with no effect or interaction involving the factors of condition and group. The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 10.54; p = .003) and site (F(4,96) = 13.17; p < .001; e = 0.351) with no other effect or interaction involving the factors of condition, laterality and group. These results indicate that ERP
Table 1 Behavioral results (SD in parentheses) Males
Females
Reaction time for correct responses (ms) New 1036.3 (247.1) Old 940.6 (218.2)
940.9 (161.4) 796.6 (105.9)
Scores % Hits % False alarms
84.4 (8.9) 12.6 (9.5)
93.7 (3.5) 6.6 (4.1)
d0
1.9 (0.6)
2.8 (0.9)
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Fig. 1. Grand averaged ERPs obtained from the midline electrode sites (Fz, Cz, and Pz) in males and females for correctly identified new items (thin lines) and correctly recognized old items (thick lines).
within the N300 time window are similarly modulated by repetition in males and females. The ANOVA on midline data for the P400 resulted in significant effects of condition (F(1,24) = 25.07; p < .001) and site (F(2,48) = 32.47; p < .001; e = 0.642). There was also a trend for a significant effect of group (F(1,24) = 3.09; p = .09) but no interaction between factors. The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 37.86; p < .001), site (F(4,96) = 31.22; p < .001; e = 0.384) and laterality (F(1,24) = 8.76; p = .007). As for the midline data, there was a trend for a significant effect of group (F(1,24) = 3.02; p = .09). As shown in Fig. 1, these results reflect that ERP amplitude is generally larger in females than in males, whereas the ERP old/new effect is similar across gender. Noteworthy, interactions between condition, site and group were present for both the midline (F(2,48) = 3.5; p = .05; e = 0.716) and lateral analyses (F(4,96) = 6.06; p = .01; e = 0.340), but they were not confirmed on scaled data. These observations suggest that gender difference in the topography of ERP old/ new effect starts within this time window. The Fig. 2 showed that the difference is larger over fronto-polar sites (Fp1, Fp2) and particularly over the right hemisphere. This could account for the observed laterality effect. The ANOVA on the midline data obtained in the N400 time window showed a significant effects of condition (F(1,24) = 70.85; p < .001), sites (F(2,48) = 34.49; p < .001; e = 0.628), and group (F(1,24) = 5.45; p = .03). There were also significant interactions between condition and group (F(1,24) = 9.31; p = .005), condition and site (F(2,48) = 5.93; p = .012; e = 0.715), and between the three factors (F(2,48) = 6.54; p = .008; e = 0.715). These results indicate that males and females differ in their the topography of their ERP old/new effect.
The Fig. 2 shows that that females displayed a larger effect than males over fronto-central sites (Fz, Cz). The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 114.51; p < .001), site (F(4,96) = 29.22; p < .001; e = 0.369), laterality (F(1,24) = 4.98; p = .04), and group (F(1,24) = 6.00; p = .02). There were also significant interactions between condition and group (F(1,24) = 13.96; p = .001), condition and site (F(4,96) = 11,00; p < .001; e = 0.395), between condition, site, and group (F(4,96) = 4.84; p = .02; e = 0.395), and between condition, laterality, and group (F(1,24) = 4.19; p = .05). Again, these results indicate a differential topography of the ERP old/new effect across genders. The Fig. 2 showed that the interactions reflect the larger effect in females at fronto-polar sites (Fp1, Fp2), particularly over the right hemisphere and the grossly similar effect over posterior sites. The ANOVA on the midline data obtained in the P600 time window showed a significant effect of condition (F(1,24) = 16.78; p < .001), sites (F(2,48) = 40.79; p < .001; e = 0.642), and group (F(1,24) = 8.80; p = .007). There were also a significant interactions between condition and group (F(1,24) = 45.60; p = .04). The Fig. 2 showed that these results reflect the generally larger ERP old/new effect in females. As in the N400 time window, the difference is more evident over fronto-central sites (Fz, Cz). The ANOVA on lateral data revealed significant effects of condition (F(1,24) = 28.941; p < .001), site (F(4,96) = 2425; p < .001; e = 0.369), group (F(1,24) = 9.88; p = .004), and a marginally significant effect of laterality (F(1,24) = 3.87; p = .06). There were significant interactions between condition and group (F(1,24) = 5.66; p = .03) and between condition, site, and laterality (F(4,96) = 9.83; p < .001; e = 0.483). Although not confirmed on scaled data, there were also
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Fig. 2. Scalp distribution of the ERP old/new effect (old minus new amplitude difference) obtained in males and females expressed in raw data in lV (left panel) and normalized data (right panel).
a significant condition · site (F(4,96) = 3.38; p < .05; e = 0.395) interaction and a trend for a condition · site · laterality · group interaction (F(4,96) = 2.49; p = .09; e = 0.483). Generally, these results indicate that the ERP old/new effect within the P600 time window is similar across genders. Nevertheless, both the additional interactions and the Fig. 2 suggest a tendency for the ERP old/new effect to be larger over right fronto-polar sites in females, as observed in the N400 time window.
4. Discussion The results on the behavioral data show that, although there is no major difference in recognition latency, between the two gender groups, females have a higher hit rate and lower false alarm rate than males. This observation replicates the general finding from the literature on gender difference in memory processing
(Herlitz et al., 1997; Herlitz et al., 1999; Ragland, Coleman, Gur, Glahn, & Gur, 2000; Silverman & Eals, 1992; Wilson & Vandenberg, 1978). In fact such a difference is observed consistently on recall and recognition tasks featuring episodic processes, such as those required for the effective processing of unfamiliar faces used here but not on working, immediate, and semantic memory tasks. In addition, the present results show the lower performance of males is mainly due to their larger number of miss responses, which suggests that they maintain less information or that they form more labile representation than females (see also Waters & Schreiber, 1991). They also tend to make more false alarms, which may indicate that the representations formed are less specific, i.e., more sensitive to subjective familiarity (see Schacter, Norman, & Koutstaal, 1998) and interference (see Kramer, Delis, Kaplan, OÕDonnell, & Prifitera, 1997; Palmer & Folds-Bennett, 1998), than in females. This interpretation is consistent with the view that females
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engage in more detailed elaboration of information that lead to more specific and less labile representation, whereas males rely on less elaborated schemas or overall information theme (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). The results of the ERP analysis show generally larger amplitudes in females than in males. This difference, present as early as the N300 and lasts until the P600, is particularly evident anteriorly (Fig. 1). This observation is comparable with that of Taylor (Taylor et al., 1990) on ERPs recorded in a non-verbal memory task, as well as with the results of some studies using simple discrimination tasks (Desrocher et al., 1995; Hoffman & Polish, 1999; Polich & Martin, 1992). As already mentioned in Section 1, the gender difference in ERP amplitudes could be related to differences in neuropil volumes (i.e., larger in females) (De Courten-Myers, 1999; Rabinowicz et al., 2002). However, neuropil difference is present in the whole brain and thus, it cannot account for the relative localization (anterior vs. posterior) and its material specificity (verbal vs. non-verbal) reported by Taylor (Taylor et al., 1990). One possibility is that the cytoarchitectural difference is better expressed in some brain regions more specifically recruited to perform in particular (experimental) conditions. In other words, task or material specific functional differences in information processing may overlap the neuroanatomical differences. This is likely to be the case since our results evidence more subtle gender differences in the modulation of the ERPs, i.e., in the old/new effect. Some spatially and temporally localized effects contributing to the general ERP old/new effects (see Section 1) display gender differences, whereas others do not. No gender difference in the ERP old/new effect is observed over posterior sites in the N400 time window. If one accepts the classical interpretation that the posterior N400 is modulated by the ease with which the incoming information is integrated with personal knowledge (i.e., the more the positive the amplitude, the easier the integration) (Holcomb, 1993; Rugg & Doyle, 1994), this result indicates that males and females perform this process as efficiently. This is in fact reminiscent with the lack of gender difference on semantic memory and priming tasks reported in behavioral studies (Herlitz et al., 1997). However, Taylor (Taylor et al., 1990) showed that in a similar task using verbal stimuli, males produced more positive ERPs over posterior sites during the N400 than females. These discrepancies are likely related to the use of different materials. Following the above interpretation of the N400, TaylorÕs results could reflect that males are more efficient than females at integrating information already represented in semantic memory, such as words. This interpretation is consistent with the view that male processing is driven mainly by preexisting schemas (Meyers-Levy & Tybout, 1989; Myers-Levy & Maheswaran, 1991). If so, no difference
should have been expected at the knowledge integration stage (i.e., N400) for stimuli that have no pre-established specific representation (except in the form of a general face schema) such as the unfamiliar faces used here. The results also show no gender difference in the ERP old/new effect on posterior P600 data. According to the classical interpretation of the P600 (Guillem et al., 2001a; VanPetten et al., 1991), this observation indicates that males and females are similarly able to bind the different aspects of information into a coherent representation. Thus, how can the differences observed on behavioral performances be accounted for? A plausible explanation is that the group differences do not differ quantitatively in the amount of information bound or retrieved as reflected in the P600 old/new effect, but in the quality of the binding that makes the representations retrievable as reflected in behavioral scores (see Guillem et al., 2001b; Guillem et al., 2003, for a similar view). As argued above, males may form more labile and less specific representations than females. In fact, if the P600 reflects the endpoint where the information extracted from the stimulus converged, the qualitative difference between genders is likely to rely on differences at antecedent processing stages those reflected in earlier ERP components. This is supported by the gender differences observed on the earlier contributors of the ERP old/new effect distributed over anterior sites. More specifically, a long-lasting gender difference is observed over fronto-polar sites from the P400 to the P600 time windows and it is likely predominating within the P400–N400 latency range as shown on normalized data (Fig. 2). This fronto-polar contributor of the ERP old/new effect has been previously related to the selection and maintenance of items in the face of interfering information (Guillem et al., 2001a). By this view, the lower effect in males indicates that they require a similar amount of interference inhibition to process old and new items. Conversely, the large effect in females indicates a facilitated processing of old items. This interpretation is consistent with the behavioral data concerning false alarms that suggested the greater interference sensitivity of males in relation with their preferential schematic or global processing of information. It is also of note that the gender difference on the fronto-polar effect is somewhat weak, as it is the case for the difference on false alarms rate. A more reliable gender difference is evidenced over fronto-central sites during the N400–P600 latency range. Interestingly, this effect is generally associated with strategic monitoring processes (Allan et al., 1998). More specifically, it could represent the processing of the intrinsic contextual attributes of items. This process is particularly critical for complex and unfamiliar stimuli that require the formation of representations that are sufficiently distinctive to be retrieved subsequently (Guillem et al., 2001a). The larger fronto-central old/
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new effect observed in females is thus, in well accordance with the view that they entail more detailed elaboration of information than males. In summary, the results of the present study obtained with ERP measures remarkably corroborate the behavioral and neuroanatomical literature concerning gender differences in memory processing. Generally, they are consistent with the idea that males and females differ in the cognitive strategies they use to process information. In addition, ERPs provide a more dynamic account in which gender differences in memory performance rely more particularly on specific stages occurring in the cascade of the cognitive and neural mechanisms involved in memory processing.
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