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• 2.1. The face location memory task
• 2.2. Participants and procedures
• 2.3.2. Spatial location memory
• 2.3.3. Male-typical spatial abilities
• 2.3.4. Intertask correlations
1. Introduction
Although the cross-species distribution of sex differences in spatial ability can be better explained by other models (e.g., Gaulin & FitzGerald, 1986, Gaulin & FitzGerald, 1989, Jacobs et al., 1990, Sherry & Hampson, 1997), the division-of-foraging-labor model (Eals & Silverman, 1994, Silverman & Eals, 1992) can explain a female advantage on object-location memory in humans. On this latter view, differential selection pressures arising from hunting versus gathering activities put a premium on different spatial competencies in ancestral men and women. Accordingly, the cognitive demands of hunting favored male spatial abilities that enhanced the capture of animals, whereas the cognitive demands of gathering plant food favored female abilities to identify the shape and color of edible plants and to locate them by remembering their proximity to landmarks (e.g., a particular tree or rock). Consistent with this formulation, a present-day male advantage is reliably documented on a variety of spatial tasks that appear to support successful hunting, including spatial navigation (Moffat, Hampson, & Hatzipantelis, 1998), mental rotation (Linn & Petersen, 1974), and the accurate aiming of projectiles (Watson & Kimura, 1991). Furthermore, in tasks developed specifically to test the evolutionary hypothesis of a female advantage for spatial location memory, women outperform men in their memory for object locations in a visual spatial array (Eals & Silverman, 1994, Silverman & Eals, 1992).
Although the activities of gathering or hunting are thought to result in divergent selection on women's and men's spatial abilities, an implicit assumption of the methods that have been used to test the theory is that the nature of the stimulus is not strongly relevant to demonstrating a sex difference in task performance. Consistent with this possibility, men's greater efficiency at mental rotation has been demonstrated in tasks using real or schematic representations of three-dimensional objects (Robert & Chevrier, 2003) and schematic representations of 2-dimensional objects (Collins & Kimura, 1997). Similarly, women show an advantage in memory for the spatial location of common household objects (e.g., Eals & Silverman, 1994), as well as abstract shapes (McGivern et al., 1998).
Whereas the male advantage in many spatial tasks has been reliably documented (Linn & Petersen, 1974, Voyer et al., 1995), less is known about the female advantage in spatial location memory. A goal of the present research was to test the hypothesis that the female advantage in location memory may generalize to a variety of stimuli by testing memory for face locations. Faces were selected as visual stimuli because, like abstract objects, faces are less compatible with verbal strategies that may afford a greater female advantage in location memory tasks (Chipman & Kimura, 1998; Galea & Kimura, 1993). The hypothesis that sex-typical spatial abilities may be evolved cognitive adaptations to foraging roles (Silverman & Eals, 1992) also implies that the female advantage in location memory does not generalize to other ‘male-typical’ spatial abilities (McBurney, Gaulin, Devineni, & Adams, 1997). For these reasons, in the present study, women and men completed a novel face location task and, for comparison, three spatial tasks that, in previous research, have shown a reliable male performance advantage.
2. Experimental methods
2.1. The face location memory task
A novel spatial memory task was constructed similar to the Silverman and Eals Location Memory task (Eals & Silverman, 1994, Silverman & Eals, 1992), which shows a female advantage in performance. Like the original location memory task, the modified memory task consisted of a stimulus card and two response cards. The stimulus card of the modified task consisted of a spatial array of 24 faces. One response array measured face recognition memory and included 20 added faces. A second response array measured face location memory and depicted the original 24 faces with an exchange between six pairs of faces. Faces varying in apparent gender and ethnicity were assembled from an assortment of face parts (i.e., noses, chins, eyes, mouths, and hairstyles) using Faces 3.0 (Interquest).
Facial expressions communicate intentions and goals (Erickson & Schulkin, 2003), and it may be advantageous to remember the locations of such faces, in particular, faces indicating personal threat. Therefore, faces with friendly, threatening, or sad emotional expressions were constructed by applying identical features to faces. A friendly expression was conveyed by an upturned mouth and eyebrows lifted in the middle. Sad and threatening expressions were conveyed by a frown and eyebrows lifted in the middle or a frown and eyebrows lowered (i.e., “V”) in the middle, respectively (Fig. 1). With these options, three versions of the Face Location Task were constructed.
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Fig. 1. Examples of sadness (A), friendliness (B) and threat (C, D). Faces A, B, and C vary in essential features of emotional expression (eyebrows, mouth). Faces C and D vary in nonessential features (e.g., hair, face shape, and nose). The construction of emotional expression is based on previous research using schematic faces (Ohman et al., 2001). |
A “neutral” condition of the Face Location Task depicted all faces with a friendly expression, consistent with previous research methods (Ohman, Ludqvist, & Esteves, 2001). Two other “negative emotion” conditions (sad and threatening conditions) depicted the same 24 faces. In the threatening condition, 16 faces displayed a friendly expression and 8 faces displayed a threatening expression. In the sad condition, 16 faces displayed a friendly expression and 8 faces displayed a sad expression. Across all three conditions, faces depicted on the response cards were uniformly friendly in their expression (i.e., a face depicted as threatening or sad on the stimulus card was depicted as friendly on the response cards). For that reason, differences in memory scores across the three conditions scores reflect the degree to which the retrieval of face identity and face location is affected by the emotional expression processed during encoding.
2.2. Participants and procedures
Participants were 60 women and 60 men between the ages of 18 and 35 years (M=20.4±1.9) who were enrolled in an introductory psychology course at Texas A&M University. All participants gave signed informed consent and received partial course credit for their participation in the protocol. All participants completed the Face Location Memory task (5–10 min), followed by a mental rotation task (5 min), a water level task (5 min), and a ball throw task (10 min), in that order.
Participants were randomly assigned to one of the three facial expression conditions of the Face Location Memory task, with the constraint that each group consisted of 20 men and 20 women. Participants were first presented with the stimulus card and told only to remember the faces. No instruction was given to attend to the emotional expression or to the location of faces. After 1 min, the stimulus card was removed. The participants were presented next with the face recognition response card and instructed to mark faces that were not on the stimulus card. After completing that task, the face location response card was presented and the participants were instructed to mark any faces that had been moved from their original positions. The time to complete the recognition and location memory tasks was recorded for each participant. Consistent with previous methods documenting the female advantage on the related Silverman and Eals object location memory task, accuracy was defined as 1−(omissions+commissions)/N.
The two-dimensional mental rotation task (Collins & Kimura, 1997), administered next, consisted of 25 items, each depicting a target figure in a random orientation with a small arrow placed directly above it. The arrow represents the hour hand of a clock at 12:00, indicating that the figure is at a 12:00 orientation. Participants must determine what the orientation of the figure would look like at a specified time ranging between 2:00 and 10:00. Next, the water level task (Tuddenham, 1970) measured the knowledge of the physical properties of water in a jar. Ten jars were presented in different orientations. Participants were asked to draw a line on the jar to represent water level. An error was defined as a deviation from the horizontal greater than 7 degrees. Dependent variables included the number of errors and the average deviation from horizontal across the 10 jars. Finally, a ball throw task (Hall & Kimura, 1995) measured targeting. The target consisted of a black square (36×36 in.) with a white dot in the center. Participants stood 10 ft from the target and threw a small ball 10 times at the white dot. No practice trials were given. Accuracy, defined as the distance, in inches, from the target center, was calculated for each of the 10 targeting trials.
2.3. Results
2.3.1. Preliminary analysis
One-sample t tests showed that the average accuracy scores for recognition and location tasks were significantly different from chance (.50) across all three conditions. Analysis of variance (ANOVA) for repeated measures on time to complete the two memory tasks showed neither sex or nor sex-by-emotional expression effects on time measures. Participants required less time to complete the location memory task (M=74.92±27.93 s) compared with the recognition memory task [M=133.40±50.96 s; F(1,114)=220.06, p<.001]. ANOVA on face recognition scores using sex and emotional expression as grouping factors showed that face recognition memory was higher in the friendly condition (M=.79±.08) compared with the sad and threat conditions [M=.69±.09 and .69±.07, respectively; F(2,114)=7.20, p<.01]. However, there were no main effects of sex [F(1,114)=0.44, p=.50] and no sex-by-facial expression interaction effect on face recognition memory scores [F(2,114)=1.5, p=.18].
2.3.2. Spatial location memory
Location memory scores were examined using ANCOVA, with facial expression condition as a between-subject factor and face recognition scores included in the model as a covariate, consistent with previous recommendations (James & Kimura, 1997). Tests of between-subject effects showed no main effect of sex but did show a significant sex-by-facial expression interaction on location memory scores [F(2,112)=6.378, p<.01]. Consistent with the predictions of Silverman and Eals (1992), a moderate female advantage in location memory (d=0.77; Cohen, 1977) occurred in the friendly condition (p<.01). In contrast, a large male advantage in location memory (d=1.23) occurred in the threatening condition (p=.05; Fig. 2).
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Fig. 2. Mean (±S.E.M.) location memory scores for men and women in each experimental group. Scores were accuracy defined as 1−(omissions+commissions)/N. The expected female advantage occurred in the friendly condition (p<.01). In contrast, a male advantage occurred in the threat condition (p<.05), and no sex difference occurred in the sad condition. |
2.3.3. Male-typical spatial abilities
A preliminary examination of means suggested group differences in the performance of other spatial tasks. For that reason, emotional expression condition was included as a grouping factor in the model, testing the effects of sex on spatial abilities. ANOVA on mental rotation scores (percent correct) showed the expected male advantage in task performance [F(1,114)=6.74, p=.01] and a sex-by-emotional expression interaction effect [F(2,114)=3.15, p=.05]. Consistent with the expected direction of sex differences in these spatial abilities, a large male advantage in mental rotation was found (d=1.19) in the friendly expression condition. However, no sex differences in mental rotation were found in either the threatening or sad conditions (Fig. 3). Within-sex comparisons showed only that women in the threat condition outperformed women in the friendly condition on the mental rotation task (p=.05).
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Fig. 3. Mean (±S.E.M.) mental rotation scores for men and women in each experimental group. The expected male advantage occurred in the friendly condition. In contrast, no sex differences occurred in the other two conditions. |
Targeting accuracy, defined as distance in inches from the center, was examined using repeated-measures ANOVA with the 10 trials as the replicates and sex and emotional expression condition as grouping factors. That analysis showed main effects of trial [F(9,106)=6.56, p=.001], sex [F(1,114)=68.98, p=.001], and emotional expression [F(2,114)=4.70, p=01]. As expected, males were more accurate than females were (d=1.4), and accuracy over trials improved in both males and females. Targeting accuracy was significantly better in the threat condition but relative only to the sad condition (p=.01). An examination of the magnitude of the sex difference (d) within the friendly (d=1.07), threatening (d=1.31), and sad (d=2.08) conditions suggests that this effect was largely attributable to women's worsened performance in the sad expression condition (Fig. 3). However, the test of that effect (i.e., the sex by facial expression interaction) was only marginally significant [F(2,114)=2.33, p=.10; Fig. 4].
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Fig. 4. Mean (±S.E.M.) accuracy scores for the 10 consecutive throws in each experimental group. Targeting in the sad expression condition was less accurate than targeting in the threat condition (p<.01). |
Water level scores (average deviation from horizontal) showed the expected male advantage in performance [F(1,144)=12.83, p<.01], of a moderate effect size (d=0.70), but no main effect of facial expression condition [F(2,144)=0.18, p=.83] or sex-by-facial expression interaction effect on performance [F(2,114)=0.51, p=.59]. A similar analysis using the number of water jar errors as the dependent measure did not change the direction or significance of these results.
2.3.4. Intertask correlations
Correlations between location memory scores and targeting accuracy, mental rotation (percent correct), and water level (deviation from horizontal) were calculated within each sex. In both males and females, better location memory was associated with poorer performance on the mental rotation task (rmen=−.275, p<.05; rwomen=−.262, p<.05). Correlations between location memory and other tasks were smaller and nonsignificant.
3. Discussion
The spatial abilities of women and men who processed friendly emotional expressions were consistent with previous reports of sex differences in human spatial abilities. Women in the friendly condition showed superior spatial location memory, whereas their male counterparts showed superior mental rotation, targeting, and displayed more accurate knowledge of the properties of water in a jar. In contrast, processing emotional expressions indicating threat resulted in a male advantage on a spatial task that typically shows a female advantage—location memory. Threat also enhanced women's performance on the mental rotation task, thereby effectively eliminating the typical male advantage on this measure. In both males and females, a brief exposure to sad facial expressions impaired subsequent performance on a targeting task.
A goal of this research was to test the hypothesis that a female advantage in spatial location memory generalizes to facial stimuli. The results for the friendly condition of a novel face location task suggest that the female advantage in spatial location does generalize—but this advantage is constrained by contextual factors. The finding that object location memory varied across emotional expression conditions is consistent with a general observation that spatial location memory in both sexes appears sensitive to stimulus features and procedural characteristics of the task (Dabbs et al., 1998, James & Kimura, 1997, McDuff & Hampson, 2000, McGivern et al., 1998, Postma et al., 1998). Previous researchers have shown that spatial location memory in males can be enhanced when male-typical items are depicted in the stimulus array (McGivern et al., 1998). In addition, males appear more sensitive to threatening facial expressions than females are (Kirouac & Dore, 1984). Therefore, men in this research may have shown better location memory in the threatening condition because threatening faces, like male-typical objects, are self-relevant. The present findings that threatening expressions enhanced an undirected memory for locations in men, but did not enhance a directed memory for face recognition, suggest that these processes are not under conscious control. Consistent with this possibility, threatening expressions characterized by eyebrows in the “V” position are known to be processed automatically, presumably because selection pressure promoted the development of specialized neural systems that respond quickly to stimuli indicating threat (Ohman et al., 2001). The results of this research suggest that a response to threat in men may include an awareness of the locations of individuals who earlier showed evidence of personal threat.
The unexpected finding that typical sex differences in spatial ability were abolished or reversed in a condition where a proportion of faces in the stimulus array depicted threatening facial expressions has implications for theories of the ontogeny of sex-linked cognitive abilities. Previous findings of reliable sex differences in adult spatial abilities (Linn & Petersen, 1974, Voyer et al., 1995) have been understood as relatively stable consequences of biosocial processes that influence the early organization and postnatal development of brain structures (or cognitive strategies) that contribute to spatial competency. The responsiveness of spatial abilities to social cues in the present study suggests that greater flexibility exists in sex-linked spatial processing than previously thought.
Social stimuli are known to alter hormone levels that may then alter sex-linked behavior (Wilson, Daly, & Pound, 2002). Brief exposure to threat, for example, may increase testosterone levels (van Honk et al., 2000), which, in turn, may influence sex-linked spatial abilities (Aleman, Bronk, Kessels, Koppeschaar, & van Honk, 2003). However, evidence of hormonal activation of spatial abilities is equivocal (Alexander et al., 1998, Liben et al, 2002). Moreover, hormonal mechanisms of behavioral change in humans appear to require a minimum of several hours to occur (Aleman et al., 2003) and, hence, could not account for the behavioral effects that were observed in this study some 3–5 min after a brief exposure to emotional faces. Instead, these data suggest that social cues are able to influence sex-linked cognitive abilities through a hormone-independent pathway of neural activation.
A hypothetical pathway between social cues and brain systems that subserve sex-typed cognitive abilities may exist because cognitive abilities facilitate reproductive goals (Gaulin, 1995, Geary, 1995, Geary, 1996). One possible explanation for the present results is that emotion activates brain areas that make differential contributions to male or female spatial abilities. In addition, recent imaging studies show that emotional processing results in sex-specific patterns of activation in the right or left amygdala (Cahill et al., 2001), a structure that also modulates brain systems (including the hippocampus) that are involved in the expression of different types of learning and memory (McGaugh, 2002, Packard et al., 1994, Packard & Teather, 1998). Sex differences in amygdala activation during emotional processing, therefore, may also contribute to the present results for spatial abilities. Clearly, future research using brain-imaging methodologies will be required to determine the network of brain areas recruited during the performance of location memory tasks. However, the present findings of sex-specific effects of emotional processing on spatial abilities permit a general conclusion that sex differences exist in the activation of brain networks integrating emotion and spatial processing. Whether this effect is dependent on the recognition of emotional states or the experience of emotional states (as a function of exposure to emotional stimuli) would be important to consider in further research of emotion and spatial abilities.
The social activation hypothesis is consistent with a general proposal that emotion promotes the attainment of adaptive goals (Geary, 1999) by facilitating situation-appropriate cognition (Chang & Wilson, 2004). Although the functional significance of the present findings cannot be determined on the basis of a single report, it may be important that emotional expressions had no effect on water level task performance, which, unlike targeting and mental rotation, appears unrelated to skills for successful hunting or fighting (Geary, 1995). Further research examining the effects of emotional cues on the performance of sex-linked tasks, for example, on spatial tasks perhaps more closely associated with the evolutionary hypotheses (e.g., a 3-D mental rotation task) or nonspatial tasks, such as verbal fluency, that typically show a female advantage, is required to fully understand what appears to be a rapid activation of spatial ability by a sex-dimorphic affective system that is responsive to the immediate demands of a social context.
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