Sex differences in visuo-spatial processing: An fMRI study of mental rotation
Introduction
1In the Shepard and Metzler mental rotation task, subjects are shown pairs of perspective drawing of 3-D regular shapes. The task of the subject on each trial is to decide whether the two shapes are identical, or if one is a mirror-image of the other (see also Cooper, 1976, Kosslyn, 1980). The typical finding is that response times increase as the angle of disparity between the two shapes increases, with requirements for cognitive processing in order to determine if they are the same shape or not. A common explanation of these findings is that an image of the shape has to be mentally “rotated” to be superimposed on the reference shape in order for the subject to decide whether the shapes are identical or not (Shepard & Cooper, 1982; Tagaris et al., 1997).
Based on behavioral responses (response accuracy) several studies have found males to perform better than females (e.g. Astur, Tropp, Sava, Constable, & Marcus, 2004; Crucian & Berenbaum, 1998; Fisher & Pellegrino, 1988; Parsons et al., 2004, Peters et al., 1995). This has been explained with reference to differences between the sexes in hemisphere functioning, with males performing better than females on typical right hemisphere processing tasks (e.g. Levy & Reid, 1978). However, not all studies have found sex differences in mental rotation. Cohen and Polich (1989) found no differences between males and females for mental rotations involving letter and polygons, i.e. different tasks than the Shepard and Metzler 3-D task.
Hooven, Chabris, Ellison, and Kosslyn (2004) measured salivary testosterone in 27 young males on a 2-day testing schedule. The results showed that increased testosterone levels had a negative effect on reaction time and error rate on the mental rotation task. The importance of the Hooven et al. (2004) study is that it identifies a biological marker for the typical male superior performance on mental rotation tasks. Similarly, Aleman, Bronk, Kessels, Koppeschaar, and van Honk (2004) found that a single administration of testosterone improved performance in young women on a mental rotation task.
The objective of the present study was to further investigate sex differences in mental rotation by means of mapping the crucial neuronal mechanisms involved. Few studies of brain activation during mental rotation thus far have systematically evaluated differences between males and females. A clear majority of published studies on brain activation to mental rotation tasks have not separated their findings for males and females (e.g. Belin, Moroni, Gelbert, Cordoliani, & Delaporte, 1998; Cohen et al., 1996, Tagaris et al., 1997, Tagaris et al., 1998, Watson et al., 1998), or only one sex has been included in the study (e.g. Jäncke et al., 1998; Richter, Ugurbil, Georgopoulos, & Kim, 1997; Taira, Kawashima, Inoue, & Fukuda, 1998). The first study that reported separate results for males and females was the study by Tagaris et al. (1996). In two more recent studies, Weiss et al. (2003) and Jordan, Wustenberg, Heinze, Peters, and Jäncke (2003), it was found that males had increased activation in the inferior parietal lobule compared to females, while females showed increased activations in frontal lobe and fusiform areas. Finally, Seurinck, Vingerhoets, de Lange, and Achten (2004), using rotated hands, found that females recruited left ventral premotor cortex. A left hemisphere effect in females was also observed by Alexander, Packard, and Peterson (2002) for memory of the locations of objects briefly presented in the left or right visual half-field.
Mental rotation paradigms are particularly suitable for studying visuo-spatial processing strategies in the right and left cerebral hemispheres. Mental rotation of abstract 3D objects are hard to verbalize, and would thus present as pure spatial tasks. Mental rotation tasks may also be conceptualized in the Kosslyn (1987) theoretical framework of categorical and coordinate metric space, pointing towards a right hemisphere processing superiority for such tasks. This is also what has been found. For example, Ditunno and Mann (1990) reported faster reaction times when the shapes were presented in the left visual field.
Similar results were reported by Corballis and Sergent (1988) when testing a patient with a surgical split of the corpus callosum, thus separating the right and left hemispheres. A more recent study by Harris, Harris, and Caine (2002) reported that patients with damage to the right basal ganglia showed significant performance deficits on a mental rotation task. However other studies on patients with unilateral, left or right hemisphere lesions (e.g. Kosslyn, Holtzman, Farah, & Gazzaniga, 1985) have found impaired performance particularly for left-hemisphere damaged patients, indicating a left hemisphere basis for mental rotation (cfr. Hellige, 1995, Kosslyn and Brown, 1995). Thus, there seem to be some contradictory points in the literature that beg for explanation. On one hand, Kosslyn's original theory posits that categorical representations are abstract and qualitatively disjoint; therefore they cannot be used to describe the continuous rigid transformations of parts and spatial rotations. In contrast, continuous rigid transformations can easily be described within a coordinate framework. Hence, mental rotation would be expected to be mainly accomplished by using coordinate, metric, representations, in a continuum of space where two spatial forms can transform into one another through intermediate orders of points. A possible solution to the paradox could be that mental rotation cannot be seen as a simple (one mechanism) process and it is in fact likely to be carried out by a system of operations working together. Particularly, comparing views of a multipart object (like the Shepard and Metzler's cubes) might require at the outset also a multipart object's structural description (i.e., representing the individual parts and their relations). In other words, although the mechanics of the rotation (the continuous transformation) might well be taking place in the right hemisphere, verbalizations or the use of verbal strategies may require the cooperation of the left hemisphere. Although the Shepard and Metzler cubes may not lend themselves too easily to verbal labels, or descriptions, it cannot be ruled out that a subject may apply some verbal labels to parts when processing the stimuli (e.g., one could label parts of the cubes shown in Fig. 1 as ‘the bottom, nearest arm’ and ‘the top, left-pointing arm’). This would explain why neuronal activations (in fMRI and PET studies) during rotation tasks are typically bilateral and why a left hemisphere lesion might compromise – in some cases more than a right hemisphere lesion – the mental rotation task.
Thus, although bilateral activations typically are found in brain imaging studies (PET and fMRI), almost all studies have also reported the right parietal lobule as involved in mental rotation, suggesting a right hemisphere processing dominance (e.g. Belin et al., 1998, Cohen et al., 1996). Other studies have, however, reported bilateral parietal lobule activation (Tagaris et al., 1996, Tagaris et al., 1997, although these authors used a different task), or inconsistent laterality across subjects (Cohen et al., 1996). Thus, the issue of hemispheric asymmetry in brain activation studies of mental rotation is unresolved yet. Part of the explanation for the variability across studies and subjects in hemispheric asymmetry for mental rotation may be the kind of baseline or control stimulus used. Both Cohen et al. (1996) and Richter et al. (1997) used the same Shepard and Metzler (1971) shapes during the experimental (mental rotation) and control conditions, subtracting fMRI images between the two conditions. However during the control condition, only non-rotated shapes were used. Although this controls for the effect of visual perception, it may induce “carry-over” processing effects from the experimental to the control stimulus condition, with the subject trying to mentally rotate also the control stimuli, since they are similar in shape and outline as the experimental stimuli. Therefore, in the present study we used different control shapes in order to optimize differences in mental rotation demands between the experimental and control conditions, while controlling for overall visual perception and for motor responses. The study of sex differences in neuronal activation in a mental rotation task is relevant also from the point of view that this has not been the topic in studies on categorical/coordinate processing.
Section snippets
Methods
Eleven right-handed healthy adults participated in an fMRI study, six males and five females (mean age 30 years, range ±10 years). Right-handedness was checked with the help of the questionnaire developed by Raczkowski, Kalat, and Nebes (1974) which consist of 14 questions related to the use of the hands and one question related to the use of the feet. All subjects participated voluntarily and gave their consent for participation before entering the MR scanner.
The subjects were presented with
Results
An analysis of variance for response accuracy and reaction time showed no significant differences between the males and females, neither for response accuracy (males 26% correct, S.D. 16%, females, 17% correct, S.D. 21%), nor for reaction time (males 3100 ms, S.D. 275 ms, females 2700 ms, S.D. 310 ms), although there was a tendency for the males to be more accurate, and the females to be faster.
For the BOLD fMRI data, there was a significant main effect of stimulus (3-D experimental versus 2-D
Discussion
A common finding in the present data with regard to visuo-spatial processing and brain function is that the task of mental rotation pre-supposes a form of coordinate metric processing in the right parietal lobe, thus supporting Kosslyn's (1987) original formulations on the nature of hemispheric asymmetry for different aspects of visuo-spatial processing. The role of the right parietal lobe, furthermore, seems to be the same for males and females, since the main sex difference was observed for
Acknowledgements
The present study was financially supported by a grant from Haukeland University Hospital to Kenneth Hugdahl. The constructive comments by Bruno Laeng on an earlier version of the manuscript are greatly acknowledged.
References (57)
- et al.
A single administration of testosterone improves visuospatial ability in young women
Psychoneuroendocriniology
(2004) - et al.
Sex and spatial position effects on object location memory following intentional learning of object identies
Neuropsychologia
(2002) - et al.
Functional activation of the human brain during mental rotation
Neuropsychologia
(1997) - et al.
Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation
Brain Behavioral Research
(2004) - et al.
Time course of fMRI activation in language and spatial networks during sentence comprhension
NeuroImage
(1999) - et al.
Imagery in a commissurotomized patient
Neuropsychologia
(1988) - et al.
Sex differences in right hemisphere tasks
Brain and Cognition
(1998) - et al.
Visuospatial tasks compared via activation of regional cerebral blood flow
Neuropsychologia
(1988) - et al.
Right hemisphere specilaization for mental rotation in normals and brain damaged subjects
Cortex
(1990) - et al.
The relationship of male testosterone to components of mental rotation
Neuropsychologia
(2004)
Sex differences in mental rotation in a virtual environment
Neuropsychologia
A redrawn Vandenberg & Kuse mental rotation test: Different versions and factors that affect performance
Brain & Cognition
Reliability and validity of some handedness questionnaire items
Neuropsychologia
Does egocentric mental rotation elicit sex differences?
Neuroimage
Functional magnetic resonance imaging of mental rotation and memory scanning: A multidimensional scaling analysis of brain activation patterns
Brain Research Reviews
Coordinate and categorical judgments in spatial imagery: An fMRI study
Neuropsychologia
Sex differences in brain activation pattern during a visuospatial cognitive task: A functional magnetic resonance imaging study in healthy volunteers
Neuroscience Letters
Categorical and coordinate spatial relations: fMRI evidence for hemispheric specialization
Neuroreport
Role of non-occipital areas in mental rotation: A fMRI Study
NeuroImage
Changes in cortical activity during mental rotation. A mapping study using functional MRI
Brain
No hemispheric differences for mental rotation of letters or polygons
Bulletin of the Pychonomic Society
Oculocentric spatial representation in parietal cortex
Cerebral Cortex
Demonstration of a mental analog of an external rotation
Perception and Psychophysics
Hemisphere differences for components of mental rotation
Brain and Cognition
Cerebral asymmetry and decision strategies in mental rotation: A psychophysical analysis
European Journal of Cognitive Psychology
Statistical parametric mapping
Spatial transformation of images
mental-rotation deficits following damage to the right basal ganglia
Neuropsychology
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