Abstract
Little is known regarding the differences in active cortical and subcortical systems during opposing movements of an agonist-antagonist muscle group. The objective of this study was to characterize the differences in cortical activation during active ankle dorsiflexion and plantarflexion using functional MRI (fMRI). Eight right-handed healthy adults performed auditorily cued right ankle dorsiflexions and plantarflexions during fMRI. Differences in activity patterns between dorsiflexion and plantarflexion during fMRI were assessed using between- and within-subject voxel-wise t-tests. Results indicated that ankle dorsiflexion recruited significantly more regions in left M1, the supplementary motor area (SMA) bilaterally, and right cerebellum. Both movements activated similar left hemisphere regions in the putamen and thalamus. Dorsiflexion activated additional areas in the right putamen. Results suggest that ankle dorsiflexion and plantarflexion may be controlled by both shared and independent neural circuitry. This has important implications for functional investigations of gait pathology and how rehabilitation may differentially affect each movement.
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Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381.
Alkadhi, H., Crelier, G. R., Boendermaker, S. H., Golay, X., Hepp-Reymond, M. C., & Kollias, S. S. (2002). Reproducibility of primary motor cortex somatotopy under controlled conditions. AJNR. American Journal of Neuroradiology, 23(9), 1524–1532.
Anderson, F. C., & Pandy, M. G. (2003). Individual muscle contributions to support in normal walking. Gait Posture, 17(2), 159–169.
Armstrong, D. M., & Drew, T. (1984). Locomotor-related neuronal discharges in cat motor cortex compared with peripheral receptive fields and evoked movements. Journal of Physiology, 346, 497–517.
Ball, T., Schreiber, A., Feige, B., Wagner, M., Lucking, C. H., & Kristeva-Feige, R. (1999). The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage, 10(6), 682–694.
Beloozerova, I. N., & Sirota, M. G. (1993). The role of the motor cortex in the control of vigour of locomotor movements in the cat. Journal of Physiology, 461, 27–46.
Capaday, C. (2002). The special nature of human walking and its neural control. Trends in Neurosciences, 25(7), 370–376.
Capaday, C., Lavoie, B. A., Barbeau, H., Schneider, C., & Bonnard, M. (1999). Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. Journal of Neurophysiology, 81(1), 129–139.
Chainay, H., Krainik, A., Tanguy, M. L., Gerardin, E., Le Bihan, D., & Lehericy, S. (2004). Foot, face and hand representation in the human supplementary motor area. NeuroReport, 15(5), 765–769.
Ciccarelli, O., Toosy, A. T., Marsden, J. F., Wheeler-Kingshott, C. M., Sahyoun, C., Matthews, P. M., et al. (2005). Identifying brain regions for integrative sensorimotor processing with ankle movements. Experimental Brain Research, 166(1), 31–42.
Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.
Dietz, V. (2003). Spinal cord pattern generators for locomotion. Clinical Neurophysiology, 114(8), 1379–1389.
Dobkin, B. H., Firestine, A., West, M., Saremi, K., & Woods, R. (2004). Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage, 23(1), 370–381.
Drew, T., Jiang, W., Kably, B., & Lavoie, S. (1996). Role of the motor cortex in the control of visually triggered gait modifications. Canadian Journal of Physiology and Pharmacology, 74(4), 426–442.
Drew, T., Kalaska, J., & Krouchev, N. (2008). Muscle synergies during locomotion in the cat: a model for motor cortex control. Journal of Physiology, 586(5), 1239–1245.
Duysens, J., & Van de Crommert, H. W. (1998). Neural control of locomotion; The central pattern generator from cats to humans. Gait Posture, 7(2), 131–141.
Earhart, G. M., & Bastian, A. J. (2001). Selection and coordination of human locomotor forms following cerebellar damage. Journal of Neurophysiology, 85(2), 759–769.
Enzinger, C., Johansen-Berg, H., Dawes, H., Bogdanovic, M., Collett, J., Guy, C., et al. (2008). Functional MRI correlates of lower limb function in stroke victims with gait impairment. Stroke, 39(5), 1507–1513.
Enzinger, C., Dawes, H., Johansen-Berg, H., Wade, D., Bogdanovic, M., Collett, J., et al. (2009). Brain activity changes associated with treadmill training after stroke. Stroke, 40(7), 2460–2467.
Gopinath, K., Crosson, B., McGregor, K., Peck, K., Chang, Y. L., Moore, A., et al. (2008). Selective detrending method for reducing task-correlated motion artifact during speech in event-related FMRI. Hum Brain Mapp.
Johannsen, P., Christensen, L. O., Sinkjaer, T., & Nielsen, J. B. (2001). Cerebral functional anatomy of voluntary contractions of ankle muscles in man. Journal of Physiology, 535(Pt 2), 397–406.
Jueptner, M., & Weiller, C. (1998). A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain, 121(Pt 8), 1437–1449.
Kapreli, E., Athanasopoulos, S., Papathanasiou, M., Van Hecke, P., Strimpakos, N., Gouliamos, A., et al. (2006). Lateralization of brain activity during lower limb joints movement. An fMRI study. Neuroimage, 32(4), 1709–1721.
Kapreli, E., Athanasopoulos, S., Papathanasiou, M., Van Hecke, P., Keleki, D., Peeters, R., et al. (2007). Lower limb sensorimotor network: issues of somatotopy and overlap. Cortex, 43(2), 219–232.
Karabanov, A., Blom, O., Forsman, L., & Ullen, F. (2008). The dorsal auditory pathway is involved in performance of both visual and auditory rhythms. Neuroimage.
Liddle, P. F., Kiehl, K. A., & Smith, A. M. (2001). Event-related fMRI study of response inhibition. Human Brain Mapping, 12(2), 100–109.
Lotze, M., Montoya, P., Erb, M., Hulsmann, E., Flor, H., Klose, U., et al. (1999). Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. Journal of Cognitive Neuroscience, 11(5), 491–501.
Luft, A. R., Smith, G. V., Forrester, L., Whitall, J., Macko, R. F., Hauser, T. K., et al. (2002). Comparing brain activation associated with isolated upper and lower limb movement across corresponding joints. Human Brain Mapping, 17(2), 131–140.
Maillard, L., Ishii, K., Bushara, K., Waldvogel, D., Schulman, A. E., & Hallett, M. (2000). Mapping the basal ganglia: fMRI evidence for somatotopic representation of face, hand, and foot. Neurology, 55(3), 377–383.
Mochizuki, G., Hoque, T., Mraz, R., Macintosh, B. J., Graham, S. J., Black, S. E., et al. (2009). Challenging the brain: exploring the link between effort and cortical activation. Brain Research, 1301, 9–19.
Nadeau, S., Gravel, D., Arsenault, A. B., & Bourbonnais, D. (1999). Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clinical Biomechanics (Bristol, Avon), 14(2), 125–135.
Neptune, R. R., Kautz, S. A., & Zajac, F. E. (2001). Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. Journal of Biomechanics, 34(11), 1387–1398.
Neptune, R. R., Sasaki, K., & Kautz, S. A. (2008). The effect of walking speed on muscle function and mechanical energetics. Gait Posture, 28(1), 135–143.
Newton, J. M., Dong, Y., Hidler, J., Plummer-D’Amato, P., Marehbian, J., Albistegui-Dubois, R. M., et al. (2008). Reliable assessment of lower limb motor representations with fMRI: use of a novel MR compatible device for real-time monitoring of ankle, knee and hip torques. Neuroimage, 43(1), 136–146.
Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.
Parent, A., & Hazrati, L. N. (1995). Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Research. Brain Research Reviews, 20(1), 91–127.
Parvataneni, K., Olney, S. J., & Brouwer, B. (2007). Changes in muscle group work associated with changes in gait speed of persons with stroke. Clinical Biomechanics (Bristol, Avon), 22(7), 813–820.
Sahyoun, C., Floyer-Lea, A., Johansen-Berg, H., & Matthews, P. M. (2004). Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. Neuroimage, 21(2), 568–575.
Schubert, M., Curt, A., Jensen, L., & Dietz, V. (1997). Corticospinal input in human gait: modulation of magnetically evoked motor responses. Experimental Brain Research, 115(2), 234–246.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thiem Medical.
Winter, D. A. (1983). Biomechanical motor patterns in normal walking. Journal of Motor Behavior, 15(4), 302–330.
Yeterian, E. H., & Pandya, D. N. (1998). Corticostriatal connections of the superior temporal region in rhesus monkeys. Journal of Comparative Neurology, 399(3), 384–402.
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This research is based upon work supported by Center of Excellence grant # B3149C and Senior Research Career Scientist Award # B3470S (to BC) from the Office of Research and Development, Rehabilitation Research and Development Service, Department of Veterans Affairs.
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Trinastic, J.P., Kautz, S.A., McGregor, K. et al. An fMRI Study of the Differences in Brain Activity During Active Ankle Dorsiflexion and Plantarflexion. Brain Imaging and Behavior 4, 121–131 (2010). https://doi.org/10.1007/s11682-010-9091-2
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DOI: https://doi.org/10.1007/s11682-010-9091-2