Increased self-monitoring during imagined movements in conversion paralysis
Introduction
Conversion paralysis (CP) is a mental disorder characterized by loss of voluntary motor functioning. Although the symptoms may suggest a neuropathological condition, they cannot be adequately explained by known neurological or other organic disorders (American Psychiatric Association, 1994). Moreover, there is an exacerbation of symptoms at times of psychological stress, which suggest that psychological mechanisms play a role.
Conversion disorder and related disorders are common in clinical practice: about one-third of new neurological outpatients exhibit medically unexplained symptoms (Carson et al., 2000; Stone, Carson, & Sharpe, 2005a). Despite the high prevalence and the long history of speculations as to the cause of CP (Halligan, Bass, & Marshall, 2001; Vuilleumier, 2005), the exact nature of CP is still not well understood. Only recently, a few studies have tried to determine objective neural correlates of functional mechanisms that, in the absence of a structural brain lesion, may be able to explain CP symptomatology. The first study to investigate the functional anatomy of conversion paralysis was by Marshall, Halligan, Fink, Wade, and Frackowiak (1997). Using positron emission tomography (PET), the authors recorded brain activity when a patient with unilateral CP tried to move either her affected or her unaffected leg. When attempting to move the unaffected (right) leg, there was a normal pattern of cerebral activity, including activation in the contralateral primary motor cortex (M1). However, when attempting to move the affected (left) leg, there was no activation in the contralateral M1, but there was a relative increase in activation of the right anterior cingulate cortex (ACC) and the ventromedial part of the prefrontal cortex (vmPFC). These results were interpreted as suggesting that the loss of voluntary movements observed in CP is caused by increased response inhibition mediated by ACC and vmPFC. Similar results were obtained in a related study, in which hypnosis was used to induce paralysis of the leg in a healthy subject (Halligan, Athwal, Oakley, & Frackowiak, 2000). When the hypnotized participant tried to move his “affected” leg, ACC and vmPFC showed increased activity, suggesting that similar mechanisms support hypnotically induced paralysis and CP (Halligan et al., 2000). In contrast, Spence, Crimlisk, Cope, Ron, and Grasby (2000) observed that when CP patients moved their paretic limb, there was a de-activation in their dorsolateral prefrontal cortex (dlPFC), as compared to healthy control subjects. Finally, Burgmer et al. (2006) did not find any differences in prefrontal or motor cortex activity between CP patients and healthy controls during execution of hand movements. Although these conflicting results may be partly due to the limited sample size (N = 1–4), and the type of comparisons carried out (within-subjects versus between-subjects), a more fundamental issue may relate to the nature of the tasks employed. Namely, in these studies, patients were asked to carry out a task (“move/try to move your affected limb”) that they could not appropriately perform due to their condition. Accordingly, it is conceivable that these results reveal cerebral effects related to the cognitive consequences of a failed movement (like altered effort, motivation, or error processing), rather than a proximal cause of CP. For instance, the increased ACC activity (Halligan et al., 2000, Marshall et al., 1997) may reflect enhanced monitoring triggered by movement failure or by conflicting action tendencies (Vuilleumier et al., 2001). This possibility is supported by our recent finding of increased action monitoring in the ACC of six unilateral CP patients during generation of movements with the affected limb (Roelofs, de Bruijn, & Van Galen, 2006).
To overcome these interpretational limitations, Vuilleumier et al. (2001) assessed brain responsiveness to sensory stimulation in CP patients suffering from unilateral sensorimotor loss. In an elegant design, both the affected and the unaffected limb were stimulated, and the cerebral responses of CP patients were measured at two time points: first, when conversion symptoms were present, and several weeks later, when the symptoms were resolved. Patients had decreased activity in the basal ganglia and thalamus contralateral to the affected limb during sensory stimulation of the affected limb compared to stimulation of the unaffected limb. This decrease resolved after recovery of conversion symptoms, suggesting that differences in sensory processing may play an important role in the pathophysiology of CP. However, it has yet to be investigated how these sensory deficits relate to the core feature of CP, namely the disturbance of volitional motor processes. Finally, a recent study explored whether CP is associated with abnormal brain activity during observation of hand movements (Burgmer et al., 2006). This study showed that compared to healthy controls, CP patients had reduced M1 activity during observation of hand movements, specifically for the affected hand. However, despite the known behavioral and neural correspondences between action observation and action execution (Grezes & Decety, 2001; Hamilton, Wolpert, & Frith, 2004), it is not trivial to link this finding to the main symptomatology of CP (limb paralysis), given that action observation does not entail an active volitional motor simulation. In the present study, we aimed to examine volitional action simulation while controlling for processes associated with actual motor execution like altered sensory feedback or enhanced monitoring of failed movements. We addressed this issue by using a motor imagery paradigm.
Using motor imagery to study the generation and preparation of actions is supported by a wealth of evidence showing that imagined and executed movements overlap in terms of time course (Parsons, 1987, Parsons, 1994, Sekiyama, 1982), autonomic responses (Decety, Jeannerod, Germain, & Pastene, 1991), and neural architecture (de Lange, Hagoort, & Toni, 2005; Jeannerod, 1994; Parsons, Gabrieli, Phelps, & Gazzaniga, 1998). Accordingly, previous behavioral studies have used motor imagery tasks to reveal impairments in motoric simulations of the affected limb in patients with CP (Maruff & Velakoulis, 2000; Roelofs et al., 2001). Here we used a well-known motor imagery task: the hand-laterality judgment task. In this mental rotation paradigm, subjects have to judge the laterality of rotated images of left and right hands. Many studies have showed that subjects solve this task by mentally moving their own hand to match the orientation of the visually presented stimulus (Parsons, 1987, Parsons, 1994). This approach allowed us to compare cerebral activity (using fMRI) evoked by motor imagery of the affected and the unaffected hand, while quantifying imagery performance. We hypothesized that, if CP entails an inhibition of the movement plan, activity should be increased in the cingulate and prefrontal cortex during motor imagery of the affected hand, while there should be a reduction of preparatory activity in motor-related structures (Burgmer et al., 2006, Marshall et al., 1997). Alternatively, if CP entails heightened action monitoring triggered by movement failure or by conflicting action tendencies (Roelofs et al., 2006, Vuilleumier et al., 2001), we expected the prefrontal hyperactivity to be accompanied by normal or even greater activity in the motor system, due to the increased effort in forming a motor plan.
Section snippets
Participants
We studied eight patients (mean age of 34.6 years, range 18–56, S.D. = 13.2) diagnosed with conversion disorder according to the DSM-IV criteria (American Psychiatric Association, 1994) and showing a full or partial paralysis lateralized to one arm as a major symptom. A criterion for inclusion was a strictly unilateral loss of motor function, clearly related to psychogenic factors and in the absence of any neurological disease (American Psychiatric Association, 1994). After referral by a
Behavioral effects
Reaction times and error rates of the participants are shown in Fig. 1. Reaction times increased with increasing stimulus rotation (main effect of rotation: F(4,28) = 10.39; p = 0.005; Fig. 1a). Trend analysis indicated that the RTs follow a combination of a linear (contrast estimate = 0.653 ± 0.072, mean ± S.E.; p < 0.001) and a quadratic (contrast estimate = 0.209 ± 0.065, mean ± S.E.; p = 0.001) increase with rotation, while no higher order trends were visible (3rd order: contrast estimate = −0.061 ± 0.053, mean ±
Discussion
In this study, we measured cerebral activity in eight CP patients with a unilateral paresis of the arm while they were engaged in a well-known motor imagery task: mental rotation of hands. Motor imagery of the affected hand and the unaffected hand recruited comparable cerebral resources in the motor system, and generated equal behavioral performance. However, motor imagery of the affected hand drew on additional cerebral resources, localized to the medial prefrontal cortex and the superior
Conclusions
Our results show that, during imagery of movements with the paralyzed arm, CP patients show similar responses in preparatory motor structures but fail to de-activate the ventromedial prefrontal and superior temporal cortex. These results suggest that the paralysis that characterizes these patients does not manifest itself at the neural level as heightened inhibition of motor processes. Rather, we observed cerebral responses that could be more readily linked to altered monitoring of movements.
Competing interests
The authors have no competing interests.
Acknowledgments
FdL and IT were supported by Dutch Science Foundation (NWO: VIDI grant no. 452-03-339). KR was supported by Dutch Science Foundation (NWO VENI grant no. 451-02-115). This study was supported by the Dutch Brain Foundation (Hersenstichting Nederland, grant number 12F04(2).19) awarded to KR and FdL. The authors would like to thank Marije van Beilen and all other colleagues for their generous assistance in recruiting patients.
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Authors contributed equally to this work.