Real versus imagined locomotion: A [18F]-FDG PET-fMRI comparison
Introduction
Erect locomotion in humans is a complex sensorimotor task requiring the dynamic interaction between spinal locomotor pattern generators and hierarchically organized supraspinal locomotion centers in the brainstem, cerebellum, and cortex. This cerebral network is believed to modulate locomotion (e.g., gait initiation, termination, velocity, direction, and spatial orientation) and to control balance and gait by integration of multisensory information (Rossignol et al., 2006). Our knowledge about the hierarchical network of supraspinal locomotion centers is derived from basic science studies mainly performed in the cat (Mori et al., 2001, Shik and Orlovsky, 1976). The most important regions are the cerebellar locomotor region (CLR), the mesencephalic locomotor region (MLR), and the subthalamic locomotor region (SLR).
In recent years functional imaging was also used to investigate human locomotion. The cortical processing of locomotion was shown by means of single-photon-emission-computed-tomography (SPECT) (Fukuyama et al., 1997, Greenstein et al., 1995), positron-emission-tomography (PET) (Ishii et al., 1995, Malouin et al., 2003, Tashiro et al., 2001), and functional magnetic resonance imaging (fMRI) (Jahn et al., 2008b, Jahn et al., 2004, Wang et al., 2008). SPECT studies of the regional cerebral blood-flow (rCBF) during walking reported brain activations in different cortical and subcortical regions known to be related to motor activity (Fukuyama et al., 1997, Greenstein et al., 1995). Only two higher resolution PET studies used [18F]-fluoro-desoxy-glucose ([18F]-FDG) to investigate the human locomotion, one after running (Tashiro et al., 2001) and one during walking on a treadmill (Ishii et al., 1995). In the latter, activation was mostly observed in the cerebellum.
More recent studies used mental imagery of locomotion and standing to investigate rCBF changes with PET (Malouin et al., 2003) and blood oxygen level-dependent (BOLD) signal alterations with fMRI (Jahn et al., 2008b, Jahn et al., 2004), because active locomotion cannot be performed in MRI or PET scanners.
In summary, a supraspinal locomotor network in humans was identified which includes the frontal cortex, basal ganglia, brainstem tegmentum and cerebellum. This network is remarkably similar to the feline locomotor network (Jahn et al., 2008a, Jahn et al., 2008b).
Despite the existing functional imaging studies on locomotion, the locomotor network of the entire brain has so far not been investigated during real locomotion. Furthermore, although the imagery of movements has been suggested to correspond well to real sensorimotor activations (Deiber et al., 1998, Lacourse et al., 2005, Porro and Cavazzuti, 1996, Stippich et al., 2002), mental imagery of locomotion in fMRI has not been directly compared to real human locomotion. Therefore, in the present study we propose a new approach for investigating brain activation during real steady-state locomotion using [18F]-FDG PET and qualitatively compare our findings with BOLD response in fMRI during imagined locomotion in the same group of subjects. This is essential for future studies especially on patients with cerebral gait disorders.
Section snippets
Subjects
Sixteen right-handed healthy adults (seven women, aged between 51 and 73 years, mean age: 61.3 ± 7.8 years) without gait disorders were included in the study. All patients underwent a complete neurological and neuro-ophthalmological examination. Posturography was performed using a Kistler-platform as has been described earlier (Krafczyk et al., 2006). All tests revealed normal results in the subjects. Vertigo and balance disorders in the patient's past medical history were excluded by a
Results
The study focused on changes in glucose metabolism shown by [18F]-FDG-PET of the whole brain during real locomotion of a group of 16 healthy subjects and compared with the results of mental imagery of locomotion in the same group revealed by fMRI. Relative changes of glucose metabolism were depicted in comparison to the individual resting condition, which indicated brain activation and deactivation specific for the locomotion task (see Table 1). Imagined locomotion was compared to imagined
Discussion
The direct qualitative comparison of real and imagined locomotion in the same group of subjects yielded the following major findings: (1) A locomotion network consisting of motor/premotor and multisensory cortices, the parahippocampal gyri and midline cerebellum is active during both real locomotion ([18F]-FDG-PET) and mental imagery of locomotion (fMRI). (2) These activations are associated with deactivations in the multisensory vestibular cortical areas in both real and imagined locomotion.
Acknowledgments
The study was supported by the German Research Foundation (JA 1087/ 1-1). We thank Thomas Stephan and Virgina Flanagin for methodical support, Judy Benson for copyediting the manuscript, Sabine Esser for graphic design and Katrin Richter for the superb technical support.
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Both authors contributed equally.