Elsevier

NeuroImage

Volume 41, Issue 3, 1 July 2008, Pages 998-1010
NeuroImage

Cerebral correlates of motor imagery of normal and precision gait

https://doi.org/10.1016/j.neuroimage.2008.03.020Get rights and content

Abstract

We have examined the cerebral structures involved in motor imagery of normal and precision gait (i.e., gait requiring precise foot placement and increased postural control). We recorded cerebral activity with functional magnetic resonance imaging while subjects imagined walking along paths of two different widths (broad, narrow) that required either normal gait, or exact foot placement and increased postural control. We used a matched visual imagery (VI) task to assess the motor specificity of the effects, and monitored task performance by recording imagery times, eye movements, and electromyography during scanning. In addition, we assessed the effector specificity of MI of gait by comparing our results with those of a previous study on MI of hand movements. We found that imagery times were longer for the narrow path during MI, but not during VI, suggesting that MI was sensitive to the constraints imposed by a narrow walking path. Moreover, MI of precision gait resulted in increased cerebral activity and effective connectivity within a network involving the superior parietal lobules, the dorsal precentral gyri, and the right middle occipital gyrus. Finally, the cerebral responses to MI of gait were contiguous to but spatially distinct from regions involved in MI of hand movements. These results emphasize the role of cortical structures outside primary motor regions in imagining locomotion movements when accurate foot positioning and increased postural control is required.

Introduction

The neural control of locomotion is complex, requiring interactions between locomotor rhythm generation, balance control, and adaptation of the movements to motivational and environmental demands. Studies in cats and rodents have shown that while the production of the basic locomotor rhythm is largely dependent upon activity of central pattern generators within the spinal cord (Dietz, 2003, Grillner and Wallen, 1985), real-life gait also depends upon supra-spinal structures that are involved in adapting walking movements to environmental and motivational demands (Armstrong, 1988). In humans, little is known about the cerebral control of gait. Lesion studies have not been particularly informative, given that cerebral lesions causing higher-level gait disorders are typically multiple, or diffuse (Masdeu, 2001). Transcranial magnetic stimulation has provided electrophysiological evidence that the motor cortex is involved in the control of ankle muscles during walking (Petersen et al., 2001). Similarly, near-infrared spectroscopy has shown specific metabolic responses around the medial aspects of the central sulcus during actual gait (Miyai et al., 2001). In addition, single photon emission computed tomography studies have revealed that cerebral structures outside the primary motor cortex – such as the premotor cortex, parietal cortex, basal ganglia and cerebellum – are also contributing to gait (Fukuyama et al., 1997, Hanakawa et al., 1999). However, since these studies examined actual gait, they could not distinguish whether those effects were related to the feedforward control of gait or to changes in somatosensory feedback during gait. This issue is an instance of the general distinction that has been drawn between processes leading to the generation of a motor plan (that include predictions of the sensory consequences of the action), and processes related to the evaluation of sensory feedback (Blakemore and Sirigu, 2003, Grush, 2004, Wolpert et al., 1998). In this conceptual framework, it appears relevant to examine the cerebral structures specifically involved in the generation of the motor plan in the absence of sensory feedback due to movement execution. Here we have used motor imagery to address this issue. More specifically, given that precision gait (like passing a narrow door, or walking along uneven ground) relies on feedforward control more than normal gait (Hollands et al., 1995, Hollands and Marple-Horvat, 1996), we have examined the cerebral structures involved in motor imagery of both normal and precision gait.

Motor imagery, i.e. the mental simulation of an action without its actual execution (Jeannerod, 1994, Jeannerod, 2006), has been widely used to study the generation of a movement plan in the absence of sensory feedback (Lotze and Halsband, 2006). This approach relies on the notion that motor imagery involves the generation of a complete motor plan that is prevented from operating on the body (Grush, 2004, Jeannerod, 1994) (for a recent review of empirical support for this notion see Jeannerod, 2006). For instance, it has been shown that the current state of one's own body influences motor imagery performance (de Lange et al., 2006, Parsons, 1994, Shenton et al., 2004, Sirigu and Duhamel, 2001), and that motor imagery, motor preparation, and motor execution share cerebral and physiological correlates (Deiber et al., 1998, Lang et al., 1994, Porro et al., 1996, Roth et al., 1996, Stephan et al., 1995).

A few studies have already examined the cerebral structures involved in motor imagery of gait (Jahn et al., 2004, Jahn et al., 2008, Malouin et al., 2003, Miyai et al., 2001, Sacco et al., 2006), including motor imagery of precision gait (Malouin et al., 2003). More specifically, it was shown that when subjects imagine walking through a series of narrow passages their metabolism increases in the precuneus, the left supplementary motor area (SMA), the right inferior parietal cortex, and the left parahippocampal gyrus compared to when they imagine walking without any obstacles (Malouin et al., 2003). However, it remains unclear which of these cerebral structures is specifically involved in imagining precision gait, rather than spatial navigation, changes in walking direction, or visual imagery processes [see also Sacco et al., 2006]. In addition, these and other studies could not provide objective behavioural evidence that the subjects were specifically engaged in motor imagery of gait during the experiment. More generally, it is important to test whether the brain regions active during imagery of gait are part of a cerebral circuit dedicated to the control of gait, or whether imagery evokes general action plans that are not influenced by the specific effector involved in the action (Glover, 2004, Johnson et al., 2002). Imagery of flexion/extension of toes and fingers recruits separate precentral regions [Ehrsson et al., 2003, see also Stippich et al., 2002], and also imagery of more complex whole body and upper extremity movements reveals a homuncular organization in the primary sensorimotor cortices (Szameitat et al., 2007). However, it remains to be seen whether a similar homuncular somatotopic organization can be found outside the motor strip, and whether it is present for motor imagery of gait.

In this study, we have used a validated motor imagery protocol for examining the cerebral correlates of motor imagery of both normal and precision gait in humans (Bakker et al., 2007, Stevens, 2005). We asked subjects to imagine walking along visually presented paths of two different widths and five different distances that evoked either normal walking (broad path) or exact foot placement and increased postural control (narrow path). This manipulation allowed us to isolate behavioural and cerebral responses that were influenced by the different environmental constraints associated with imagining walking on supports of different size, distinguishing these responses from the generic effects associated with imagining walking along different distances. Furthermore, we assessed the motoric specificity of the cerebral and behavioural effects by using a matched visual imagery task, in which subjects imagined a disk moving along the same paths and distances used in the motor imagery tasks. Finally, we assessed the effector specificity of motor imagery of gait by comparing it with motor imagery of hand movements (de Lange et al., 2006).

Section snippets

Subjects

Sixteen healthy men (age 22 ± 2 years, mean ± SD) participated after giving written informed consent according to the Declaration of Helsinki. All subjects had normal or corrected-to-normal vision, and no neurological or orthopaedic disturbances. All participants were consistent right-handers (Edinburgh Handedness Inventory (Oldfield, 1971) score 84 ± 12%, mean ± SD). The study was approved by the local ethics committee.

Experimental set-up

During the experiment, subjects were lying supine in the MR scanner. Head movements

Behavioural performance

There were no significant differences in imagery times between the two tasks (main effect of TASK: (F(1,14) = 2.9, p = 0.1). In both tasks, IT increased with increasing path length (main effect of PATH LENGTH: F(1.1,15.6) = 155.3, p < 0.001 — Figs. 3a,b). Crucially, the effect of path width on IT differed for the different tasks (TASK × PATH WIDTH interaction: F(1,14) = 39.5, p < 0.001). A smaller path width resulted in longer IT in the MI task (F(1,14) = 37.0, p < 0.001) (Fig. 3a), but had no effect on IT in

Discussion

In this study we examined the cerebral structures involved in motor imagery of normal and precision gait. We distinguished imagery-related effects influenced by environmental constraints from generic imagery-related effects, and controlled for changes in muscle activity. We found that the activity and the inter-regional couplings between bilateral SPL, the dorsal precentral gyri, and the right sMOG were modulated by the degree of spatial accuracy of the imagined gait movements, with activity

Conclusion

Our results show that motor imagery of gait results in increased activity in the PMd, RCZp, SPL, and putamen. In addition, the increased spatial accuracy required to imagine walking along a narrow path increases cerebral activity bilaterally in the SPL and in the right SMOG, together with increased effective connectivity between these regions and the dorsal premotor areas controlling foot movements. These results emphasize the role of cortical structures outside primary motor regions in

Acknowledgments

This research was supported by the Stichting Internationaal Parkinson Fonds (to MB and BB). BB was supported by the Netherlands Organisation for Scientific Research (NWO: VIDI grant no. 91776352). FdL and IT were supported by the Netherlands Organisation for Scientific Research (NWO: VIDI grant no. 45203339). RCH was supported by the Alkemade–Keuls foundation. We would like to thank Paul Gaalman for his expert assistance during scanning.

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