The man who executed “imagined” movements: Evidence for dissociable components of the body schema

Abstract

We examined the nature of representations underlying motor imagery and execution in a patient (CW) with bilateral parietal lesions. When imagining hand movements, CW executed the imagined motor act but was unaware of the movements. These movements were significantly more accurate than volitional movements for the left but not right hand. CW also exhibited preserved motor imagery for the left but not right hand. Consistent with previous accounts, these findings suggest that motor imagery may normally involve the inhibition of movements. CW’s unawareness of movements during motor imagery may reflect inattention or misattribution of the unexpected sensory feedback. Furthermore, in line with current models of motor control, motor imagery may depend on the integrity of a “forward model” derived from motor outflow information to generate a prediction of the consequences of a motor command. Such predictions appear to be preserved for imagery of left but not right hand movements in CW. Action may additionally depend on precise updating of effector position derived from the comparison of predicted and actual sensory information. We propose that CW’s impaired volitional movements may be attributable to the degradation of such an updating mechanism.

Introduction

Converging evidence from neuroimaging and psychophysical investigations suggests that both real and imagined movements may depend on similar processes. For example, several recent positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) investigations have revealed similar patterns of neural activity involving areas underlying motor planning (i.e., dorsolateral prefrontal cortex, inferior frontal cortex, and the posterior parietal cortex) as well as motor execution (i.e., motor cortex, premotor cortex, lateral cerebellum, and basal ganglia) for both motor imagery and motor execution tasks (Decety et al., 1994; Grafton, Arbib, Fadiga, & Rizzolatti, 1996; Lotze et al., 1999; Parsons & Fox, 1998; Porro et al., 1996; Roth et al., 1996; Stephan et al., 1995). Further, based on extensive psychophysical investigations demonstrating strong correlations between the times required to simulate and execute movements, Parsons (e.g., 1987 and 1994) has suggested that simulated movements may depend on the same on- line representation of body movement and position that guides actual movements. Parsons and Fox (1998, p. 586) state, “In summary, motor imagery appears generally to involve the same movement representation used by the executive motor processes—a unitary representation of movements as they occur, in accordance with the physical laws underlying motor control and implementing all physiological and pathophysiological constraints.” In agreement with this account, several investigators have suggested that the mental representations underlying motor imagery and execution differ primarily in that inhibitory processes suppress motor output during imagery (e.g., Lotze et al., 1999; Decety, 1996; Jeannerod, 1994).

However, Sirigu and colleagues have observed that while normals and patients with motor cortex damage display strong correlations between the times required to imagine and execute sequential finger movements, times for patients with parietal damage are poorly correlated (Sirigu et al., 1995, Sirigu et al., 1996). These findings suggest that the parietal cortex may be an important component of the neural substrate underlying motor imagery ability and, critically, that the representations underlying motor imagery and motor execution may differ in at least some respects.

Additional evidence supporting this claim comes from several observations. For example, Sirigu, Daprati, Pradat-Diehl, Franck, and Jeannerod (1999) recently demonstrated that patients with left parietal damage are impaired relative to controls on a task that requires them to determine whether observed finger movements are being executed by themselves or by the examiner. The patients were more likely to claim that movements executed by the examiner were actually executed by themselves even when the movements made by the examiner did not precisely match the movements made at the same time (but out of sight) by the patient. For example, one patient, after a poorly executed movement, falsely attributed the well-executed movement made by the examiner to herself and exclaimed, “Tiens j’ai réussi cette fois!” (“Look, this time I succeeded!”). These findings were interpreted as indicating an impaired ability to compare an on-line representation of sensory feedback concerning finger movements with an internally generated representation of the planned finger movements (such a comparison is termed the “Sensory Comparator” and is shown in Fig. 1 and described below).

Reports of illusory movements in patients with anosognosia for hemiplegia (i.e., unawareness and explicit denial of hemiplegia) are also relevant in this context (Babinski, 1914; Feinberg, Roane, & Ali, 2000; Levine, Calvanio, & Rinn, 1991). For example, Feinberg et al. (2000) reported that after being asked to raise their plegic arms, 5 of 11 anosognosic patients reported raising their arm despite no actual movement. Further, Heilman, Barrett, and Adair (1998) observed a patient suffering from a right hemisphere stroke who claimed that when he attempted to move his contralateral arm he could feel it moving. As noted by these investigators, such confabulations concerning movements of a plegic limb suggest that some patients with anosognosia may deny their hemiplegia because they misconstrue neural activity associated with the planning of an intended movement as evidence of actual movement (in terms of the model illustrated in Fig. 1, may be a confusion between “Predicted Movement” and the “Proprioception/Sensation Feedback” resulting from actual hand movement). Thus, while the denial of hemiplegia is expressed in linguistic terms, the underlying cause of anosognosia for hemiplegia, on this account, is thought to be mediated not by language, but instead by a failure to discriminate between representations of predicted movements and representations of movement derived from sensory feedback. Consistent with this account, we recently observed a patient (JD) with left posterior parietal damage who exhibited impaired pointing accuracy (without vision) following passive movements of her arm, but a relatively preserved ability to update her pointing trajectory after active movements of her arm (Schwoebel, Coslett, & Buxbaum, 2001). For example, JD was able to point to the remembered position of a visual target after actively moving her hand to her nose, but was unable to point to the same target after the examiner moved her hand to her nose. These results suggest a possible dissociation between an on-line representation of movement derived from sensory information (i.e., Proprioception/Sensation Feedback), which appears to be impaired in JD, and an internally generated model of predicted movement (i.e., Predicted Movement), which appears to be relatively intact in JD.

In addition to evidence suggesting that predicted movements and sensory feedback from movements may be integrated (i.e., in a Sensory Comparator) in order to generate precise updates of effector location, there is also evidence suggesting that predicted hand movements are normally derived from two main sources: motor outflow/efference copy information and initial sensory inflow information. This type of prediction is analogous to predicting whether shooting a basketball will be successful based on the motor command used to launch the ball and the initial observed trajectory of the ball. For movements, such a prediction, such as the final position of the hand when attempting to reach to a target, may be integrated with target location information in order to provide on-line corrective feedback during a reaching movement (Bard et al., 1999; Desmurget et al., 1999; Desmurget & Grafton, 2000; Van Sonderen, Gielen, & Denier, 1989; Wolpert, Ghahramani, & Jordan, 1995). For example, Bard et al. (1999) demonstrated that a deafferented patient could correct reaching trajectories, despite not being able to view her moving limb, in a double-step task in which target location was changed during the ocular saccade. Such corrections suggest the modification of initial motor commands based on forward models derived solely from motor outflow information. Importantly, the more accurate corrections made by control subjects suggest that forward models based on the integration of motor outflow and sensory inflow may normally produce better predictions of hand movement/location.

As illustrated in Fig. 1, which was adapted from Desmurget and Grafton (2000) and Wolpert et al., 1995, the above findings suggest the possibility that on-line information about the position of the body in space—a level of representation which we (Buxbaum, Giovannetti, & Libon, 2000; Coslett, 1998; Schwoebel et al., 2001) and others (e.g., Head & Holmes, 1911–1912) have termed the “body schema”—may be composed of distinct representational modules.

Initial sensory inflow (e.g., Proprioception/Sensation) may be integrated with Motor Outflow information in a Forward Model that, in turn, generates a prediction or estimate of the dynamic and sensory consequences of a planned movement (i.e., Predicted Movement). Such a prediction may subsequently be compared with target location information in order to provide on-line corrective feedback to motor commands (i.e., Motor Error Signal). Additionally, the Predicted Movement may also be integrated (i.e., Sensory Comparator) with actual sensory information (i.e., Proprioception/Sensation Feedback) in order to generate a precise update of effector location (i.e., Updated Hand Location). We suggest that the components of this model that comprise the body schema (in bold) are the Initial Hand Location, Forward Model, Predicted Movements, Sensory Comparator, and the Updated Hand Location in that they are all critical to the accurate dynamic estimation of body position. Further, while we note that distinctions between the control of reaching and finger movements (i.e., grasping) have been proposed (Arbib, 1981), we suggest that these movements may be coordinated (Jeannerod, Arbib, Rizzolatti, & Sakata, 1995) and may rely on body schema processes similar to those outlined above.

An important point to be noted in this context is that imagined movements differ in a critical way from executed movements in that they normally do not involve actual movement. Thus, while motor imagery and action may both be dependent on the generation of predicted movements, the forward model for action may be derived from both sensory and motor outflow information, while the forward model generated during motor imagery may depend primarily on motor outflow information. Further, only action is expected to involve the integration of predicted and actual sensory information by the sensory comparator. Indeed, as discussed further below, there is evidence suggesting that sensory information may normally be attenuated during motor imagery in order to reduce conflicting signals regarding movement (Craver-Lemley & Reeves, 1992).

We report data relevant to this account of the differences between motor imagery and motor execution. The investigations were motivated by initial observations of a patient (CW) with bilateral parietal lesions who generated movements, without awareness, while “imagining” such movements. Importantly, these movements appeared to be more fluid, precise, and effortless than movements generated with volition. First, we document our initial observations concerning CW’s failure to inhibit movements and unawareness of movements of both hands during motor imagery tasks. We also demonstrate, in two different tasks, that movements of CW’s left hand during imagery were more precise than volitional movements of the left hand. No differences were observed for right hand movements. Second, we examine the possibility that the impaired volitional left hand movements might be attributable to faulty updating of hand position due to the degradation of the Sensory Comparator.