Elsevier

NeuroImage

Volume 47, Issue 3, September 2009, Pages 1026-1037
NeuroImage

Motor inhibition in hysterical conversion paralysis

https://doi.org/10.1016/j.neuroimage.2009.05.023Get rights and content

Abstract

Brain mechanisms underlying hysterical conversion symptoms are still poorly known. Recent hypotheses suggested that activation of motor pathways might be suppressed by inhibitory signals based on particular emotional situations. To assess motor and inhibitory brain circuits during conversion paralysis, we designed a go–nogo task while a patient underwent functional magnetic resonance imaging (fMRI). Preparatory activation arose in right motor cortex despite left paralysis, indicating preserved motor intentions, but with concomitant increases in vmPFC regions that normally mediate motivational and affective processing. Failure to execute movement on go trials with the affected left hand was associated with activations in precuneus and ventrolateral frontal gyrus. However, right frontal areas normally subserving inhibition were activated by nogo trials for the right (normal) hand, but not during go trials for the left hand (affected by conversion paralysis). By contrast, a group of healthy controls who were asked to feign paralysis showed similar activation on nogo trials and left-go trials with simulated weakness, suggesting that distinct inhibitory mechanisms are implicated in simulation and conversion paralysis. In the patient, right motor cortex also showed enhanced functional connectivity with the posterior cingulate cortex, precuneus, and vmPFC. These results suggest that conversion symptoms do not act through cognitive inhibitory circuits, but involve selective activations in midline brain regions associated with self-related representations and emotion regulation.

Introduction

Conversion disorders have been observed in medical practice for many centuries but the exact cognitive and emotional processes as well as the underlying neurophysiological substrates remain poorly known (Kozlowska, 2005, Vuilleumier, 2005, Vuilleumier, 2009). Formerly called “hysteria” in classic psychiatry terminology, conversion is defined by the presence of neurological symptoms (such as paralysis, anesthesia, blindness and so forth) that cannot be attributed to organic brain injury but appear to be triggered by particular emotional stressors or conflicts. Importantly, these symptoms are not consciously feigned by the patient in order to obtain help or gain, but rather thought to result from some distortion of bodily functions in self-awareness. The notion of “conversion” was inspired by the influential work of Freud and Breuer (1895), who proposed that physical symptoms might reflect psychological motives or affective motive (often related sexual issues) that are unconsciously repressed and then transformed into bodily complaints with some symbolic meaning. This view was partly derived from the earlier work of Charcot (1892) and Janet (1894) who insisted on the role of a dissociation between conscious and unconscious processes, with the latter overtaking the former for the control of mental or sensorimotor functions.

Although the Freudian account of hysterical conversion did not make reference to any specific cerebral mechanisms underlying the production of physical symptoms, Charcot and several other theorists after him have speculated on the possible neural pathways by which emotional states might affect the mind and behavior of these patients. Charcot himself considered that the functioning of the nervous system could be altered without any visible pathology under the influence of powerful ideas, suggestions, or psychological states, in a manner similar to the effect of hypnosis (Charcot, 1892), while his student Babinski added that such factors could produce conversion in specific individuals based on the personal meaning of emotional triggers and idiosyncratic predispositions (Babinski and Dagnan-Bouveret, 1912). Others have proposed that conversion might represent a pathological exaggeration of some primitive forms of reflexive behavior in response to psychological or physical stressors (Kretschmer, 1948, Whitlock, 1967). An early account for these phenomena in terms of specific neural mechanisms was proposed by Pavlov (1941) who speculated that an over-excitation of “subcortical centers” due to strong emotions might lead to a response of cortical inhibitory processes (tentatively located in frontal lobe) whose regulatory action could then overflow to other systems and somehow “switch off” sensorimotor functions. Similarly, several subsequent theorists suggested that the pseudo-neurological deficits in hysterical conversion (such as paralysis, anesthesia, or blindness) might result from a selective “blockade” or “gating” of sensorimotor inputs, either at the level the thalamus (Ludwig, 1972, Sackeim et al., 1979) or through the action of attentional mechanisms mediated by anterior cingulate or parietal cortex (Marshall et al., 1997, Sierra and Berrios, 1999, Spiegel, 1991). Other more recent accounts suggested a disconnection between ongoing sensory or motor representation and self-awareness processes mediated by central executive systems in prefrontal cortex (Oakley, 1999), or a by distortion of sensory or motor representation due to emotional states or past experiences (Brown, 2004, Damasio, 2003).

However, until recently, very few studies have used direct neurophysiological measures such as EEG, MEG, or functional brain imaging to provide direct support for these theoretical accounts of conversion (Vuilleumier, 2005, Vuilleumier, 2009). A pioneer study used SPECT in a single female patient with left arm anesthesia (Tiihonen et al., 1995) and reported abnormal hemispheric asymmetries with decreased activity in right parietal areas and increases in right frontal areas during left sensory stimulation, but these results did not suggested specific causal mechanisms for such changes. A subsequent influential study was conducted by Marshall et al. (1997) in another single patient who suffered from chronic leg weakness since a few years, and was asked to attempt to move one of the other leg on command during PET imaging. Results showed that unlike a normal left motor activation for executed movements with the right leg, attempts of movements with the left/paralyzed leg did not only produce no activation in right motor cortex but activated orbitofrontal and anterior cingulate areas instead, a finding that was taken to suggest that voluntary actions were prevented due to an active inhibition of motor pathways by ventromedial prefrontal areas. Subsequently, several other studies using fMRI have also reported decreases activations in motor (Burgmer et al., 2006, Kanaan et al., 2007, Stone et al., 2007), sensory (Ghaffar et al., 2006, Mailis-Gagnon et al., 2003), or visual regions (Werring et al., 2004) in conversion patients with paralysis, anesthesia, or blindness, respectively, often together with concomitant increases in medial or dorsolateral prefrontal areas. Another study reported reduced activation of thalamus and basal ganglia contralateral to the limbs affected by motor and sensory conversion symptoms during passive vibratory stimulation (Vuilleumier et al., 2001), which returned to normal symmetric levels after remission of the symptoms. Network connectivity analyses in these patients further revealed that subcortical decreases were functionally coupled with changes in ventral prefrontal areas (BA 11/BA 45), suggesting that the latter brain regions might provide a source for modulatory influences on the basal ganglia-thalamic loops controlling voluntary movement (Haber, 2003, Vuilleumier et al., 2001).

While these studies generally converge to demonstrate that conversion symptoms may lead to functional changes in brain areas concerned with the affected sensorimotor domain, it still remains unclear which areas within prefrontal cortex are most specifically implicated, and whether their activity corresponds to inhibitory processes or to other attentional or motivational functions (see Ballmaier and Schmidt, 2005, Sierra and Berrios, 1999, Vuilleumier, 2009). Thus, changes in anterior and cingulate medial prefrontal areas in conversion have also been related to increased self-monitoring and ferror processing (de Lange et al., 2007, Roelofs et al., 2006; Vuilleumier et al., 2001). Another study comparing patients with conversion and feigned paralysis during a motor task found reduced activation in left dorsolateral prefrontal cortex in the former case, but in right dorsolateral prefrontal cortex in the latter case (Spence et al., 2000b), and these changes were attributed to disturbances in mechanisms underlying conscious will and the internal generation of motor intentions (Spence, 1999). Such disturbances might potentially accord with impairments in covert planning of motor actions during mental imagery (de Lange et al., 2008, Maruff and Velakoulis, 2000) or action observation (Burgmer et al., 2006) in some conversion patients. Nevertheless, because conversion symptoms remit with sedation and distraction, their production might be consistent with a role of active inhibition or monitoring processes mediated by prefrontal executive systems (Oakley, 1999, Spiegel, 1991). Hence, taken altogether, current imaging data have not fully determined the exact neural networks involved in conversion and the exact functional role of changes in prefrontal regions.

Here we used fMRI in a patient with unilateral conversion paralysis to directly test whether her motor deficit involved inhibitory processes subtended by anterior and medial prefrontal areas, and whether these were similar or not to those responsible for conscious inhibition in normal conditions (and/or to those recruited during simulation). We designed a new go–nogo paradigm that allowed us to probe for different aspects of motor preparation, execution, and inhibition within a single task, for both the intact and affected hand. Go–nogo paradigms have been extensively used to study motor inhibition and are known to recruit selective brain regions, particularly the right inferior frontal gyrus (Aron et al., 2004, Garavan et al., 1999). In our study, by comparing performance in a go–nogo task in normal conditions and during motor conversion affecting one hand, we could determine whether voluntary inhibition of an action (e.g. nogo condition for a “normal” hand) and conversion paralysis (e.g. go condition for a “paralyzed” hand) would share similar neural mechanisms (i.e., activation of right IFG). In addition, by combining go–nogo responses with a motor preparation phase, during which participants must prepare a hand movement prior to the imperative Go or NoGo cue, we could also test whether conversion paralysis involved a suppression of motor intention, i.e., a selective loss of volition for the affected limb. If the internal generation of motor actions is impaired (Spence et al., 2000b), then the preparation phase should evoke no motor activation for the paralyzed hand (and no subsequent inhibition). Alternatively, if conversion paralysis results from active inhibition of willed movement (Marshall et al., 1997), then activation of motor and premotor areas should arise normally during preparation, while inhibitory activity should arise at the time of execution (e.g. left-go trials should actually correspond to the nogo conditions). Finally, if conversion involves a functional dissociation between discrete brain networks supporting executive and sensorimotor functions (Oakley, 1999), then the connectivity patterns of motor regions should differ between conversion and normal conditions, or between the affected and normal hand side. Importantly, to determine effects specific to conversion, we also investigated a control group of healthy subjects who were instructed to simulate a unilateral hand paralysis.

Section snippets

Participants

The patient was a 36-year-old right-handed woman, divorced with two young children and with several recent stressful life events, including a new relationship break-up. She had a degree in psychology but was not currently working. She was initially admitted to the hospital for acute and transient gastro-abdominal symptoms (diarrhea and vomiting) of probable viral origin. She had no psychiatric or neurological history, except a minor post-traumatic neck pain several years ago that recovered

Behavioral performance

In the normal condition, healthy participants correctly responded with both hands for GO (97.4%) as well as NOGO conditions (96.9%). During simulation, performance was also highly accurate with the right hand for GO (95.8%) and NOGO trials (96.4% respectively), whereas no movement was made with left hand, indicating successful compliance with our instruction in the simulator group. Likewise, RTs on correct GO trials with the right hand were similar in both control groups (normal condition and

Discussion

By systematically comparing different aspects of motor control (preparation, execution, inhibition) during a go–nogo task, we were able to test for several hypotheses concerning the neural mechanisms of unilateral hand paralysis in a patient with conversion. Our results reveal that conversion does not involve an active inhibition of motor outputs by inhibitory control systems subserved by anterior or medial prefrontal regions such as IFG or ACC. Rather, conversion produced selective changes in

Acknowledgments

We thank François Lazeyras for his help during data collection. This research is supported by grants of Cogito Foundation to PV and YC, Ernest-Boninchi Foundation to PV and LW and the Academic Society of Geneva (Foremane) for PV.

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