Imagined rotations of self versus objects: an fMRI study

Abstract

This study used functional magnetic resonance imaging (fMRI) to investigate the neural mechanisms underlying two types of spatial transformations: imagined object rotations and imagined rotations of the self about an object. Participants viewed depictions of single three-dimensional Shepard–Metzler objects situated within a sphere. A T-shaped prompt appeared outside of the sphere at different locations across trials. In the object rotation task, participants imagined rotating the object so that one of its ends was aligned with the prompt. They then judged whether a textured portion of the object would be visible in its new orientation. In the self rotation task, they imagined rotating themselves to the location of the T-prompt, and then judged whether a textured portion of the object would be visible from the new viewpoint. Activation in both tasks was compared to respective control conditions in which identical judgments were made without rotation. A direct comparison of self and object rotation tasks revealed activation spreading from left premotor to left primary motor (M1) cortex (areas 6/4) for imagined object rotations, but not imagined self rotations. In contrast, the self rotation task activated left supplementary motor area (SMA; area 6). In both transformations, activation also occurred in other regions. These findings provide evidence for multiple spatial-transformation mechanisms within the human cognitive system.

Introduction

If a person wants to know what an object looks like from a different viewpoint without actually moving, there are at least two mental transformations she can try. She can imagine rotating the object until the desired viewpoint is aligned with her current perspective, or she can imagine moving herself around the object to the new viewpoint. Both of these mental transformations are important in everyday tasks of spatial reasoning. Each requires the representation of a different spatial reference frame. Imagined object rotations involve transformation of the object-relative reference frame, which specifies the location of an object's parts with respect to each other (Easton & Sholl, 1995). Imagined self rotations involve transformation of the egocentric reference frame, which specifies an object's location and orientation with respect to the intrinsic axes of the observer's body (Howard, 1982). The egocentric frame also can be specified at smaller scales to relate objects to specific parts of the body, such as the head or hand.

An important question is whether the mental transformations associated with object-relative and egocentric reference frames are subserved by different neural mechanisms. If different neural systems are activated during the two types of transformation, this is solid evidence that different mechanisms are in play. In recent years, researchers have used neuroimaging techniques to explore this issue. Most studies have examined imagined object rotations (e.g., Barnes et al., 2000; Carpenter, Just, Keller, Eddy, & Thulborn, 1999; Cohen et al., 1996; Kosslyn, DiGirolamo, Thompson, & Alpert, 1998; Lamm, Windischberger, Leodolter, Moser, & Bauer, 2001; Richter et al., 2000, Tagaris et al., 1997, Vingerhoets et al., 2001). Some have examined imagined rotations of bodies (e.g., Creem et al., 2001a). The few studies directly comparing both classes of mental rotation have yielded ambiguous evidence for distinct mechanisms (Zacks, Ollinger, Sheridan, & Tversky, 2002; Zacks, Rypma, Gabrieli, Tversky, & Glover, 1999; Zacks, Vettel, & Michelon, 2003). In the present study, we used functional magnetic resonance imaging (fMRI) to identify the neural substrates underlying imagined self and object rotations, using novel rotation tasks.

The first hints that different spatial transformations may be subserved by different mechanisms were evident in behavioral studies that compared how easily participants can imagine rotating an array versus how easily they can imagine rotating themselves around the array (e.g., Amorim & Stucchi, 1997; Creem, Wraga, & Proffitt, 2001b; Huttenlocher & Presson, 1997; Presson, 1982; Wraga, Creem, & Proffitt 2000; Wraga, Creem-Regehr, & Proffitt, 2004). In these experiments, participants typically perform one or the other type of imagined rotation and then update the location of a given object in an array. Researchers consistently have found faster and more accurate performance during imagined self rotations than during imagined rotations of the array. Moreover, the response time (RT) functions corresponding to each type of imagined rotation show unique characteristics. RTs for imagined array and object rotations tend to increase linearly when greater amounts of rotation are required, which suggests that observers mentally transform objects similarly to the way objects are physically transformed (Shepard & Metzler, 1971). In contrast, RTs for imagined self rotations usually are independent of rotation magnitude beyond 0°, with the exception of angles that are oblique to the intrinsic axes of the body (Wraga, 2003, Wraga et al., 2000, Wraga et al., 2004). Performance also is unaffected by physically impossible situations, such as imagining rotating one's body around an array that is parallel to a wall (Creem et al., 2001b). Thus, although they conform to some physical laws constraining the body, imagined self rotations generally exhibit more flexibility than their physical counterparts.

Neuroimaging studies have begun to elucidate the neural correlates of imagined self and object rotations. For mental rotation of objects, it is well established that the posterior parietal lobules play a major role. Many studies have found bilateral posterior parietal activation, with the greatest concentration in the left superior parietal lobule (area 7) (e.g., Kosslyn et al., 1998, Richter et al., 2000, Tagaris et al., 1997, Vingerhoets et al., 2001). Recent studies have begun to delimit the precise function of the superior parietal lobule in mental rotation (e.g., Harris & Miniussi, 2003; Podzebenko, Egan, & Watson, 2002). For example, Podzebenko et al. (2002) used fMRI to demonstrate that changes in cerebral blood flow within the superior parietal lobule are positively correlated with the magnitude of rotation of a mentally rotated object. This finding suggests that the superior parietal lobule is intimately involved in the process of altering the representation of an object's orientation per se, perhaps by mapping transformations of the object-relative reference frame.

Some neuroimaging studies also have provided evidence that low-level motor areas (specifically, premotor and primary motor [M1] areas) are activated during mental rotation. Investigators initially reported motor activation for mental transformations of body-related stimuli such as hands and feet. They interpreted these findings as evidence that participants had imagined rotating their own body parts to solve the tasks (e.g., Bonda, Petrides, Frey, & Evans, 1995; Kosslyn et al., 1998, Parsons et al., 1995). However, a growing number of studies have reported motor activation during mental rotation of nonbody objects (e.g., Bonda et al., 1995, Carpenter et al., 1999, Cohen et al., 1996; Kosslyn, Thompson, Wraga, & Alpert, 2001; Richter et al., 2000, Tagaris et al., 1997, Vingerhoets et al., 2001). For example, Cohen et al. (1996) examined mental rotation of the Shepard and Metzler (1971) figures with fMRI and found premotor activation in half of their participants. Using positron emission tomography (PET), Kosslyn et al. (2001) examined whether participants could voluntarily adopt motor strategies during mental rotation. Kosslyn et al. found that the primary motor area M1 was activated when participants were instructed to solve a mental rotation task by imagining objects being turned by their hands; in contrast, no such activation occurred when participants imagined the objects being rotated by an external source, such as an electric motor. Such activation of motor areas also has been shown to transfer implicitly from an imagined hand rotation task to an object rotation task (Wraga, Thompson, Alpert, & Kosslyn, 2003). Richter et al. (2000) provided evidence that motor activation is not epiphenomenal to the mental rotation process, but rather plays an integral part. They found that peak activation in motor areas correlated positively with participants’ RTs in a mental rotation task. These findings suggest that low-level motor activation plays a role in the process of mentally rotating nonbody objects, perhaps by transforming spatial signals from the posterior parietal lobule into movement signals (see also Ganis, Keenan, Kosslyn, & Pascual-Leone, 2000; Harris & Miniussi, 2003; Snyder, Batista, & Andersen, 2000; Wexler, Kosslyn, & Berthoz, 1998).

The mechanisms underlying imagined self rotations are less well understood. Creem et al. (2001a) used fMRI to examine performance in an imagined self rotation task. Participants memorized the locations of four objects in an array, and then updated the objects’ locations after performing imagined “log-roll” transformations of their bodies about the array's center. Similar to mental rotation of objects, Creem et al. found bilateral superior parietal activation with stronger activation in the left cerebral hemisphere. They also reported left premotor area (PMA; area 6) and supplementary motor area (SMA; area 6) activation, but no M1 activation. Zacks et al. (2002) attempted to directly compare imagined object and self rotations using fMRI. In their study, participants viewed stimuli of human bodies and performed two mental rotation tasks. In one, participants made same-different judgments of a pair of bodies misoriented with respect to each other, essentially treating the bodies as objects to be rotated into congruence. In the other, participants judged whether one of two bodies had a right or left arm extended, a task requiring an egocentric transformation. Both tasks elicited typical areas of activation found in mental rotation tasks, including bilateral activation in superior parietal lobules and in premotor areas. However, a direct comparison yielded no distinctive cortical regions across the two tasks, only different relative amounts of activity. In general, Zacks et al. (2002) found greater cortical activation in the same-different task versus the right-left task within the right posterior cortex.

One explanation for Zacks et al.'s (2002) failure to identify distinct brain areas that underlie the different classes of rotation is that their tasks were ambiguous. It is possible that participants construed the left-right task as an imagined hand rotation task rather than an imagined self rotation task. That is, participants may have performed the task by simply imagining rotating their hands into the stimuli, rather than imagining the perspective change required of imagined self rotations. In the present study, we designed tasks that require explicit rotations in order to identify the neural activation underlying imagined self and object rotations. Participants viewed depictions of a single object situated within a sphere and made judgments about its appearance after either imagining rotating the object or imagining rotating themselves around the object. Based on the results of previous mental rotation studies, we expected to find distinctive mechanisms for imagined object and self rotations. Specifically, we predicted that posterior parietal activation would occur in both rotation tasks, but that low-level motor area activation would be restricted to imagined object rotations.