Differential activation of the human brain during mental rotation paradigms, an fMRI study

Mental rotation tests traditionally show a male performance advantage. Some neuroimaging studies have reported sex specific cortical activation patterns during mental rotation. However, these experiments used abstract stimuli and some studies did not systematically exclude performance as a confounding variable. The mental rotation of hands and hand-related objects, compared to abstract objects, is known to evoke an egocentric motor strategy. In this study, we used fMRI to explore potential gender specific cortical activation patterns for the mental rotation of hands and tools in a sample with an adequate and equal performance for men and women. We found a common neural substrate for men and women comprising superior parietal lobe, dorsolateral premotor cortex, and extrastriate occipital areas, compatible with an egocentric motor strategy for the mental rotation of hands and tools. Sex differences were modest and limited to the mental rotation of hands. Women recruited more left ventral premotor cortex, which could imply that women rely more on imitation or use more perceptual comparisons. Men, on the other hand, drafted more the lingual gyrus, possibly referring to more extensive semantic or early visual processing. We conclude that men and women use a very similar motor strategy during egocentric mental rotation with a potential gender-specific accent. DIFFERENTIAL ACTIVATION OF THE HUMAN BRAIN DURING MENTAL ROTATION PARADIGMS | 47 48 | DIFFERENTIAL ACTIVATION OF THE HUMAN BRAIN DURING MENTAL ROTATION PARADIGMS INTRODUCTION Men outperform women on several spatial ability measures. Particularly, the Mental Rotations Test (MRT) shows a robust sex difference (Crucian and Berenbaum, 1998; Halpern and Tan, 2001; Masters, 1998; Parsons et al., 2004; Siegel-Hinson et al., 2002; Vandenberg & Kuse, 1978; Voyer et al., 1995). The MRT is a paper-and-pencil test based on the mental imagery study of Shepard and Metzler (1971). This test shows that the response time, associated with deciding whether two objects at different orientations are identical or mirrorimages, increases with angular disparity. Similar behavioral experiments have revealed that mentally rotating a visual image is very similar to physically manipulating an actual object (Cooper and Shepard, 1984; Kosslyn and Ochsner, 1994). Why does this specific implementation of an imagery-based problem solving strategy elicit sex differences? A number of explanations have been offered within the nature or nurture debate. An illustration of the environmental approach, related to sex stereotyping, is the effect of spatial experience (Cerone and McKeever, 1998). The biological line of research, on the other hand, suggests that genetics, hormonal exposure, and cerebral organization may cause the sex difference. Kimura (1999) for example, stresses the importance of prenatal events and early or current hormonal environments, possibly mediated by brain structure and function. Up to this point, there is no consensus on the relative contribution of these two viewpoints. Though there seems to be a dominance of biological causes in the literature as illustrated by a tachistoscopic study, revealing that sex differences on the MRT were primarily due to right hemispheric specialization while spatial activity experiences were only secondarily involved (Siegel-Hinson et al., 2002). A recent study distinguishes task variables besides environmental causes and biological factors (Parsons et al., 2004). Task variables have long been discarded but may prove to be important. For instance, the manner of administrating and scoring the MRT influences the effect size of the sex difference (Voyer et al., 1995). One could also wonder if the nature of the stimulus, employed in the mental rotation task, has an impact. The MRT consists of images of threedimensional multiarmed cube shapes, originally used in the Shepard-Metzler experiment. Adjusting the complexity of these Shepard-Metzler objects still elicits sex differences (Bryden et al., 1990), but they disappear when real threedimensional models of the original images are used (Bryden et al., 1990; McWilliams et al., 1997). Studies reporting mental rotation of pictures of completely different objects, such as hands or a manikin, result in a male advantage too (Karadi et al., 2001; Richardson, 1994). Of particular interest is the study of Collins and Kimura (1997), which implies that even a two-dimensional mental rotation task utilizing simple abstract figures could bring forth a sex difference as large as on the MRT, but only if the task was difficult enough (e.g., CHAPTER 4 | MOTOR IMAGERY large angular disparity). We conclude that images of a wide variety of objects can lead to sex differences in mental rotation performance, provided that the task difficulty is sufficiently high. Underlying sex differences in brain organization are often regarded as an indication of a biological explanation for the male advantage in mental rotation. The emergence of functional brain imaging offers the possibility to directly verify if females recruit other brain regions while performing mental rotation, associated with gender-specific strategies. To our knowledge, up to now, four studies have explored sex differences in cortical activation patterns while performing a mental rotation task very similar to the MRT (Dietrich et al., 2001; Jordan et al., 2002; Thomson et al., 2000; Weiss et al., 2003). One study found larger cortical activation patterns in females, compared to males, but only during the high estrogen phase (Dietrich et al., 2001). The level of estrogen had no effect on the lateralization or localization of the cortical activation pattern. The other three experiments report gender specific cortical activation patterns, but there is no consensus on the nature of these differences (Jordan et al., 2002; Thomson et al., 2000; Weiss et al., 2003). Two studies suggest that men show increased activation of parietal areas, reflecting a gestalt strategy, while women would rather recruit right inferior frontal cortex, indicating a more analytic or serial strategy (Thomson et al., 2000; Weiss et al., 2003). Jordan et al. (2002), on the other hand, find stronger activity for women in the inferior temporal gyrus, premotor cortex, and certain parietal areas, while the men demonstrate more involvement of the primary motor cortex, a part of the left intraparietal sulcus, and the parietooccipital sulcus. In the following, we wish to focus on two aspects of these three studies: the stimuli employed and the behavioral measures reported. First, the abovementioned experiments are limited to the mental rotation of abstract stimuli. All three studies used Shepard-Metzler objects in their experimental condition. One study also included two-dimensional abstract objects and letters (Jordan et al., 2002). Mental rotation of other objects, particularly hand related stimuli, may result in a different cortical activation pattern. A PET study, comparing the mental rotation of hands and ShepardMetzler objects, resulted in stimulus-specific cortical activation patterns with motor and premotor cortex activation limited to the hands condition, reflecting a differential strategy (Kosslyn et al., 1998). Mental rotation of stimuli such as hands preferably evoke a motor strategy with imaginary limb movement, resulting in additional activation of motor areas, while abstract stimuli (e.g., Shepard-Metzler objects) are more prone to elicit a visual object transformation. These motor strategies in mental rotation could also be referred to as egocentric strategies since it has been suggested that motor strategies are not limited to the mental rotation of bodyparts but are rather required by egocentric mental DIFFERENTIAL ACTIVATION OF THE HUMAN BRAIN DURING MENTAL ROTATION PARADIGMS | 49 50 | DIFFERENTIAL ACTIVATION OF THE HUMAN BRAIN DURING MENTAL ROTATION PARADIGMS transformations in general (Wraga et al., 2003). The term “egocentric” refers in this definition to an egocentric frame of reference in both action and space, as the participant imagines the mental rotation from the first-person-perspective and experiences oneself as the agent of the mental rotation (Vogeley and Fink, 2003). In a second PETstudy (Kosslyn et al., 2001) subjects were instructed to adopt two different strategies while mentally rotating the same Shepard-Metzler objects, an egocentric strategy in which one imagines oneself as the agent of rotation or a strategy where the object is being rotated by an external or nonbody source. A direct comparison of both strategies revealed only motor cortex activity when using an egocentric strategy. A recent fMRI study comparing the mental rotation of hands and tools in a male sample, further demonstrated that these egocentric or motor strategies can also be implicitly evoked by graspable, handrelated objects (Vingerhoets et al., 2002). The mental rotation of hands evoked bilateral premotor involvement, suggesting imaginary movement for both hands to solve the task, while the mental rotation of tools revealed unilateral premotor activation associated with the dominant hand, implying imaginary manipulation of the tool with this hand. We can summarize that an egocentric strategy in mental rotation implies imaginary limb movement with its corresponding cortical activation pattern and can be elicited implicitly through hand-related stimuli. Second, these three studies report behavioral data pertaining to the performance on the mental rotation task. Behavioral measures are important for two reasons. To start with, they allow to control whether participants actually used mental rotation to solve the task. In other words, is the error rate sufficiently small and does the response time increase with angular disparity? Second, a SPECT study, using a related visuospatial task, suggests that quality of performance, rather than gender, has an effect on the cortical activation pattern (Unte