Brain correlates of hypnotic paralysis—a resting-state fMRI study
Highlights
► Altered representation of self and motor abilities during hypnotic paralysis. ► Dissociation of MPFC and PCC/PCu connectivity during hypnotic paralysis. ► Major role of PCC/PCu for altered representation of self and motor abilities.
Introduction
In recent years, hypnosis has become a new promising tool to investigate normal and pathological mental conditions in cognitive neuroscience (Oakley and Halligan, 2009). Induction of hypnosis provokes an altered state of consciousness, characterized by a subjective “increase in absorption, focused attention, disattention to extraneous stimuli and a reduction in spontaneous thought” (Lynn et al., 1996). Specific instructions in the hypnotic state can influence the mental self-representation of the subject leading to e.g. altered sensory experience or motor control. Depending on the responsiveness of the subject, suggestions in the hypnotic state can even evoke the illusion of a paralysed body part. Based on the observation that both hypnotic paralysis as well as hysterical paralysis are not explained by neurological lesions and are not intentionally produced, Oakley (1999) hypothesized that both types of paralysis may be explained by a common model involving a central executive structure acting outside self-awareness, which can be directly influenced by internal and external sources. Blakemore and Frith demonstrated the presence of such an internal self-representation which is only partly available to awareness and further argued that a distortion of this system may induce psychopathological symptoms such as delusions (Blakemore et al., 2002, Blakemore, 2003a, Blakemore, 2003b). Nevertheless, it remains poorly understood to date which neurobiological mechanisms are involved when cognitive alterations produce a motor paralysis. Therefore, the present study was performed to examine the neurobiological correlates of hypnotic paralysis.
Hypnotic paralysis has so far only been investigated in three imaging studies. Halligan et al. (2000) reported a single-case PET study of a 25-year-old man with hypnotically induced paralysis of his left leg. When the participant attempted but failed to move the left leg, activation of right orbito-frontal (Brodman area [BA] 10/11) and anterior cingulate (BA 32) cortex, but not of the motor cortex, was demonstrated. Ward et al. investigated 12 subjects with hypnotically induced paralysis of their left legs, again using PET. They observed relative increases in brain activation in the right orbito-frontal cortex, right cerebellum, left thalamus, and left putamen compared to intentionally simulated paralysis. In contrast to Halligan et al., they did not detect activation of the right anterior cingulate cortex (Ward et al., 2003). Finally, Cojan et al. reported a functional magnetic resonance imaging (fMRI) study in 12 healthy volunteers who performed a go/nogo task while their left hand was hypnotically paralysed. The authors observed preparatory activation in right motor cortex indicating preserved motor intentions, but with associated increases in the precuneus and enhanced functional connectivity between the precuneus and the right motor cortex. Their results suggest that hypnotic paralysis does not primarily act through direct motor inhibition, but that “hypnosis induces the control of action by internal representations generated through suggestion and imagery, mediated by precuneus activity, and reconfigures the executive control of the task implemented in the frontal lobes” (Cojan et al., 2009b). Interestingly, these conclusions parallel those of our group concerning patients with conversion paralysis. As Cojan et al., we did not observe a direct inhibitory mechanism preventing motor action in conversion paralysis, but reported a dysfunction of motor representation during passive movement observation (Burgmer et al., 2006). The motor task used by Cojan et al.(2009b) highlighted an increased coupling between the primary motor cortex (M1) and the left dorsal part of the precuneus and the right angular gyrus during hypnosis. Whether functional connectivity of M1 is also altered in the resting state remains unclear so far.
As previous studies emphasized the contributory role of medial prefrontal areas (Halligan et al., 2000, Ward et al., 2003) and the precuneus (Cojan et al., 2009b) – both belong to the so-called default mode network (DMN) – during experimental conditions in hypnotic paralysis, we were interested in functional alterations of these areas during the resting-state. The DMN is the most considered and stable resting-state network which can be reliably measured by correlation based analyses (Greicius et al., 2003, Nir et al., 2006, Shehzad et al., 2009, Waites et al., 2005, Yan et al., 2009), independent component analysis (Beckmann et al., 2005, DeLuca et al., 2006, Greicius et al., 2004, Kim et al., 2009, Meindl et al., 2009) and by contrasting rest and task conditions (Binder et al., 1999, Mason et al., 2007, Singh and Fawcett, 2008, Tamás Kincses et al., 2008, Vuontela et al., 2009). The DMN involves a highly correlated network in the low-frequency range (< 0.1 Hz) of the blood oxygen level dependent (BOLD) signal, including the medial prefrontal cortex (MPFC), dorsolateral frontal regions, the medial parietal cortex, particularly the posterior cingulate cortex and precuneus (PCC/PCu), and the bilateral inferior parietal cortex. Besides performance-dependent deactivation during a task (Broyd et al., 2009, Giambra, 1995, Gusnard et al., 2001, Mason et al., 2007, McKeown et al., 1998, McKiernan et al., 2003), DMN activity at rest seems to be affected by preceding events as well (Pyka et al., 2009, Schneider et al., 2008). For example, DMN activity during rest is increased after a preceding working-memory task with increased cognitive load (Pyka et al., 2009). The degree of self-relatedness to presented images is correlated with the activation of the ventro- and dorsomedial prefrontal cortex and the posterior cingulate cortex in the subsequent rest phase (Schneider et al., 2008). Furthermore, subjects shifting from a pure resting state to a movement-readiness condition revealed a stronger functional coupling of the lower part of the precuneus with an upper area of the precuneus and motor related cortices (Treserras et al., 2009). Considering that further studies found the precuneus to be involved in motor execution and imagery (Hanakawa et al., 2003, Hanakawa et al., 2008, Meister et al., 2004, Wager et al., 2004) and functionally connected with motor areas in hysterical conversion paralysis (Cojan et al., 2009a), the DMN, and in particular the precuneus, appears to be the controlling unit when prospective thoughts and self-referential processes include motor related actions.
Neuroanatomically, the MPFC and the medial parietal cortex, especially the PCC/PCu, are the core regions of the DMN. The MPFC has been suggested to integrate emotional and cognitive processes (Bush et al., 2000, Gusnard and Raichle, 2001, Simpson et al., 2001a, Simpson et al., 2001b) and is involved with the regulation of complex emotional behaviours such as decision making and calculating the value of rewards, also in social contexts (Bechara et al., 2000, Hare et al., 2010, Marco-Pallarés et al., 2010). Furthermore, MPFC is active during mentalization of actions (Marsh et al., 2010, Spunt et al., 2010). Beyond that, evidence from resting-state studies suggests a role of the MPFC for self-referential processes (Rameson et al., 2009, van Buuren et al., 2010). The PCC/PCu encompasses several highly interconnected regions which have traditionally received little attention (Cavanna and Trimble, 2006, Margulies et al., 2009). These regions are involved in highly integrated tasks such as visuo-spatial imagery, episodic memory retrieval, self-referential processes and consciousness (Cavanna and Trimble, 2006, Cavanna, 2007, Rameson et al., 2009, van Buuren et al., 2010). Thus, MPFC and PCC/PCu functions have been roughly characterized, pointing to different functional roles of the DMN.
In order to further characterize the neurobiological correlates of hypnotic paralysis, we performed resting-state fMRI both during hypnotic suggestion of left-arm paralysis and in the wake state. We assumed that the suggestion of hypnotic paralysis, first using metaphors such as “the left hand feels weak, heavy, adynamic,” “any energy leaves the hand” and then using direct instructions like “the left hand is paralysed, you cannot move the hand anymore,” modulates the perception of the self, which is represented in the resting brain. More specifically, we assumed that an altered state of self-perception in hypnotic paralysis particularly affects the perception of the subjects own motor abilities, represented in connected motor, memory and action controlling areas. Therefore, we performed connectivity analyses for the bilateral MPFC, PCC/PCu and M1 to explore if cerebral coupling of these regions is altered during hypnosis. Based on previous literature, we specifically assume an involvement of the precuneus in the maintenance of hypnotic paralysis.
Section snippets
Subjects
Healthy student volunteers recruited by advertisement were enrolled in the study. The subjects were carefully screened prior to the study and only participated in the experimental fMRI procedure if they
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were right-handed according to the Edinburgh handedness scale (Oldfield, 1971)
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reported no neurological illness or impairment
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did not fulfil any psychiatric disorder according the SCID-I interview (Wittchen et al., 1997)
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were not taking regular medication or drugs
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furthermore did not show signs of
Functional localizer task
Statistical analysis of the motor task in the non-hypnotic state revealed during imitation of a hand movement increased activity of the contralateral M1, the medial supplementary motor area, bilateral visual cortex (V5) and a cluster in the ipsilateral cerebellum. Fig. 2 depicts clusters of increased BOLD activity in the primary motor cortex during imitation of a moving hand (versus the control condition). Left-hand movement during the non-hypnotic state caused the greatest response in M1
Discussion
We performed a resting-state study to further characterize the neurobiological correlates of hypnotic paralysis, exploring functional connectivity of two regions of the default mode network (DMN) and M1 on the representation level of the left and right hand. While MPFC and M1 connectivity did not reveal any changes in the hypnotic condition, connectivity of the PCC/PCu with a bilateral superior area of the PCC/PCu and the right dorsolateral prefrontal cortex was significantly increased during
Conclusion
In conclusion, functional connectivity analysis on the resting state revealed that hypnotic suggestion of a left-hand paralysis leads to an increased coupling of the PCC/PCu with areas of cognitive control and motor representation, while MPFC and M1 connectivity remained unchanged by hypnotic paralysis. Our study suggests that induction of a hypnotic paralysis is neurobiologically paralleled by strengthened couplings between different anatomical areas, based on complex network properties,
Acknowledgments
This work was supported by a scholarship to M.P. by the Otto Creutzfeld Center for Cognitive Neuroscience, University of Münster, Germany, and by a young investigator grant to C.K. by the Interdisciplinary Centre for Clinical Research of the University of Münster, Germany (IZKF FG4).
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