Elsevier

NeuroImage

Volume 23, Issue 3, November 2004, Pages 1020-1026
NeuroImage

Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study

https://doi.org/10.1016/j.neuroimage.2004.07.002Get rights and content

We investigated changes of regional activation in the frontal cortices as assessed by changes of hemoglobin oxygenation during walking at 3 and 5 km/h and running at 9 km/h on a treadmill using a near-infrared spectroscopic (NIRS) imaging technique. During the acceleration periods immediately preceded reaching the steady walking or running speed, the levels of oxygenated hemoglobin (oxyHb) increased, but those of deoxygenated hemoglobin (deoxyHb) did not in the frontal cortices. The changes were greater at the higher locomotor speed in the bilateral prefrontal cortex and the premotor cortex, but there were less speed-associated changes in the sensorimotor cortices. The medial prefrontal activation was most prominent during the running task. These results indicate that the prefrontal and premotor cortices are involved in adapting to locomotor speed on the treadmill. These areas might predominantly participate in the control of running rather than walking.

Introduction

Experimental studies have indicated that bipedal gait is controlled by the cerebral cortices including motor neurons in the medial portion of the primary motor cortex (Ferrier, 1876, Leyton and Sherrington, 1917, Penfield, 1950) as well as the spinal central pattern generators and multiple motor centers in the brainstem (Armstrong, 1988, Drew, 1988, Mori et al., 2001, Nutt et al., 1993). In human gait, a study using single photon emission computed tomography showed activation in the multiple areas including the supplementary motor area, medial sensorimotor cortex, striatum, and cerebellum (Fukuyama et al., 1997). A near-infrared spectroscopic (NIRS) imaging study revealed that walking at the pace of 1 km/h on a treadmill was associated with a bilateral increase of oxygenated hemoglobin (oxyHb) in the medial sensorimotor cortices and the supplementary motor areas (Miyai et al., 2001). However, it is unclear whether there is also a significant relationship between cerebral activation and physiological parameters of gait such as speed and cadence. It is also not known how the rostral regions in the frontal cortices, such as the prefrontal and the premotor cortex, are involved in locomotor control, In the elderly, walking improved the performance of cognitive tasks involving prefrontal executive functions, such as a switching task, a response compatibility task, and a stopping task to abort a preprogrammed action (Kramer et al., 1999). A study has shown that habitual jogging improves a branching task combining the main visuospatial delayed-response and subroutine go/no-go task associated with the anterior prefrontal function (Harada et al., 2004, Koechlin et al., 1999). In patients with hemiparetic stroke, enhanced premotor activation in the affected hemisphere was associated with locomotor recovery (Miyai et al., 2002, Miyai et al., 2003). Thus, we hypothesized that the prefrontal and premotor cortices are involved in the control of human walking and running. To test this hypothesis, we evaluated cortical activation patterns associated with locomotor speed as assessed by relative changes of oxyHb and deoxygenated hemoglobin (deoxyHb) levels using an optical imaging technique. Our results indicated that the prefrontal–premotor regions and sensorimotor cortices are activated differentially during walking and running and that the prefrontal activation is prominent, especially during running.

Section snippets

Subjects and tasks

A total of nine, right-handed, healthy subjects (seven males, two females; mean age ± SD, 28.1 ± 7.4 years; range 22–46 years) without known neurological abnormalities participated in the experiments. This study was approved by the Ethical Committee of Bobath Memorial Hospital, and a written informed consent was obtained from each subject. The subjects performed three types of locomotor tasks (walking at 3 and 5 km/h, and running at 9 km/h) on a treadmill (Model 3200; SportsArt Ind., WA). Fig. 1

Data analysis

Changes of hemoglobin concentration were represented as mMol·cm. These data were sampled at the rate of 190 ms. Since previous findings (Hoshi et al., 2001, Strangman et al., 2002, Wolf et al., 2002) and our own findings (Miyai et al., 2001, Miyai et al., 2002) have shown that oxyHb was the most sensitive marker for task-related hemodynamic changes, we used oxyHb levels for the assessment of regional cortical activation. We derived data and made calculations from 42 channels from the “ΔoxyHb

Results

As locomotor speed increased from 3, 5, and then 9 km/h, cadence significantly increased linearly, and the heart rate and blood pressure increased slightly after 3 and 5 km/h walking, but the increase was greater after 9 km/h running. Sao2 was affected by none of the tasks (Table 1). Fig. 3 illustrates representative data for temporal changes of oxyHb, deoxyHb, and totalHb during locomotor tasks at different speeds in the PFC, PMC, m-SMC, and l-SMC.

In the PFC, PMC, and m-SMC, oxyHb and totalHb

Discussion

During the 13-s periods that immediately preceded reaching the constant locomotor speed on the treadmill, the PFC and PMC activation tended to increase as locomotor speed and cadence increased. Interestingly, the m-SMC activation appeared to be unchanged or decreased as the locomotor speed increased. In contrast, several previous studies have demonstrated a linear correlation between regional cerebral blood flow (CBF) in the hand area of the human primary motor cortex and the rate or amplitude

Conclusion

Multiple motor areas including the PFC, PMC, and m-SMC were activated during the periods before reaching a constant speed of walking and running. The prefrontal and premotor cortex might be involved in controlling locomotion to adapt to the increasing speed in the acceleration phases.

Acknowledgments

This work was supported by Funds for the Comprehensive Research on Aging and Health and Medical Frontier Strategy Research from the Ministry of Health, Labor and Welfare in Japan. We thank H. Eda and H.C. Tanabe from the Communications Research Laboratory for technical assistance with the 3D-MRI study and H. Yagura, M. Arita, and colleagues from the Rehabilitation Department of Bobath Memorial Hospital for technical assistance with the NIRS measurement.

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