Abstract
Echoplanar fMRI was used to measure changes in cortical activation during the performance of a simple hand movement task under three types of voluntary control. Each of three imaging series alternated a task with rest: passive (in which the experimenter moved the hand), voluntary against low resistance, and voluntary against higher resistance. Contralateral activation was observed in the supplementary motor area (SMA), the primary motor cortex (M1), and the somatosensory cortex (S1) in all three tasks in each subject, whereas ipsilateral activation differed in each cortical region for each task. SMA had the widest prevalence of ipsilateral activation in all three tasks. In the M1, ipsilateral activation was observed in all but 1 subject in the two voluntary tasks but in only a few subjects in the S1 in any of the tasks. Quantitative changes in signal intensity and spatial extent of activation differentiated the voluntary tasks from the passive task and were most pronounced in the S1.
Article PDF
Similar content being viewed by others
References
Alexander, G. E., & Crutcher, M. D. (1990). Preparation for movement: Neural representation of intended direction in three motor areas in the monkey. Journal of Neurophysiology, 64, 133–150.
Ashe, J. (1997). Force and the motor cortex. Behavioural Brain Research, 87, 255–269.
Baker, J. R., Weisskoff, R. M., Stern, C. E., Kennedy, D. N., Jiang, A., Kwong, K. K., Kolodny, L. B., Davis, T. L., Boxerman, J. L., Buchbinder, B. R., Wedeen, V. J., Belliveau, J. W., & Rosen, B. R. (1994, August). Statistical assessment of functional MRI signal change. Paper presented at the Annual Meeting of the International Society for Magnetic Resonance in Medicine, San Francisco.
Bandettini, P. A., Jesmanowicz, A., Wong, E. C., & Hyde, J. S. (1993). Processing strategies for time-course data sets in functional MRI of the human brain. Magnetic Resonance in Medicine, 30, 161–173.
Bandettini, P. A., & Ungerleider, L. G. (2001). From neuron to BOLD: New connections. Nature Neuroscience, 4, 864–866.
Beierlein, M., Gibson, J. R., & Connors, B. W. (2000). A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nature Neuroscience, 3, 904–910.
Bernard, R. A., Carr, T. H., Goran, D. A., McFarlane, D., Cooper, T. G., & Potchen, E. J. (1999, April). Activity in sensorimotor cortex during simple hand movements: Comparing passive experience of motion to endogenous control of action. Paper presented at the Cognitive Neuroscience Society, Washington, DC.
Bernard, R. A., Goran, D. A., Cooper, T. G., Meyer, R. A., Egger, T. J., Backus, M. A., Putnam, C. M., Paonessa, P. D., Carr, T. H., & Potchen, E. J. (1995, August). Cortical localization of somatic sensory and motor responses: A functional MRI study. Paper presented at the 3rd Annual Meeting of the International Society for Magnetic Resonance in Medicine, Nice.
Bullmore, E., Brammer, M., Williams, S. C. R., Rabe-Hesketh, S., Janot, N., David, A., Mellers, J., Howard, R., & Sham, P. (1996). Statistical methods of estimation and inference for functional MR image analysis. Magnetic Resonance in Medicine, 35, 261–277.
Cheney, P. D., & Fetz, E. E. (1980). Functional classes of primate corticomotoneuronal cells and their relation to active force. Journal of Neurophysiology, 44, 773–791.
Colebatch, J. G., Deiber, M.-P., Passingham, R. E., Friston, K. J., & Frackowiak, R. S. J. (1991). Regional cerebral blood flow during voluntary arm and hand movements in human subjects. Journal of Neurophysiology, 65, 1392–1401.
Cox, R. W., Jesmanowicz, A., Wong, E. C., & Hyde, J. S. (1995). Real-time functional magnetic resonance imaging. Magnetic Resonance in Medicine, 33, 230–238.
Deiber, M.-P., Passingham, R. E., Colebatch, J. G., Friston, K. J., Nixon, P. D., & Frackowiak, R. S. J. (1991). Cortical areas and the selection of movement: A study with positron emission tomography. Experimental Brain Research, 84, 393–402.
Dettmers, C., Connelly, A., Stephan, K. M., Turner, R., Friston, K. J., Frackowiak, R. S., & Gadian, D. G. (1996). Quantitative comparison of functional magnetic resonance imaging with positron emission tomography using a force-related paradigm. Neuro-Image, 4, 201–209.
Dettmers, C., Fink, G. R., Lemon, R. N., Stephan, K. M., Passingham, R. E., & Frackowiak, R. S. J. (1995). Relation between cerebral activity and force in the motor areas of the human brain. Journal of Neurophysiology, 74, 802–815.
Donoghue, J. P., Sanes, J. N., Hatsopoulos, N. G., & Gaal, G. (1998). Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. Journal of Neurophysiology, 79, 159–173.
Evarts, E. V. (1968). Relation of pyramidal tract activity to force exerted during voluntary movement. Journal of Neurophysiology, 31, 14–27.
Evarts, E. V., Fromm, C., Kroller, J., & Jennings, V. A. (1983). Motor cortex control of finely graded forces. Journal of Neurophysiology, 49, 1199–1215.
Evarts, E. V., & Tanji, J. (1974). Gating of motor cortex reflexes by prior instruction. Brain Research, 71, 479–494.
Fetz, E. E., Finocchio, D. V., Baker, M. A., & Soso, M. J. (1980). Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. Journal of Neurophysiology, 43, 1070–1089.
Flament, D., & Hore, J. (1988). Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey. Journal of Neurophysiology, 60, 1268–1284.
Friston, K. J., Jezzard, P., & Turner, R. (1994). The analysis of functional MRI time series. Human Brain Mapping, 1, 153–171.
Galea, M. P., & Darian-Smith, I. (1994). Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cerebral Cortex, 4, 166–194.
Georgopoulous, A. P. (2000). Neural mechanisms of motor cognitive processes: Functional MRI and neurophysiological studies. In M.S. Gazzaniga (Ed.), The new cognitive neurosciences (2nd ed., pp. 531–537). Cambridge, MA: MIT Press.
Georgopoulos, A. P., Ashe, J., Smyrnis, N., & Taira, M. (1992). The motor cortex and the coding of force. Science, 256, 1692–1695.
Ghez, C., & Krakauer, J. (2000). The organization of movement. In E. Kandel, J. H. Schwartz, & T. M. Jessell (Eds.), Principles of neural science (pp. 653–673). New York: McGraw-Hill.
Gould, H. J., Cusick, C. G., Pons, T. P., & Kaas, J. H. (1986). The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor and the frontal eye fields in owl monkeys. Journal of Comparative Neurology, 247, 297–325.
Grafton, S. T., Woods, R. P., & Mazziotta, J. C. (1993). Within-arm somatotopy in human motor areas determined by positron emission tomography imaging of cerebral blood flow. Experimental Brain Research, 95, 172–176.
Grosbras, M.-H., Lobel, E., VandeMoortele, P.-F., LeBihan, D., & Betholz, A. (1999). An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cerebral Cortex, 9, 705–711.
Heeger, D. J., & Ress, D. (2002). What does f MRI tell us about neuronal activity? Nature Reviews: Neuroscience, 3, 142–151.
Hepp-Reymond, M.-C., Wyss, U. R., & Anner, R. (1978). Neuronal coding of force and the rate of force change in the pre-central finger region of the monkey. Experimental Brain Research, 7 (Suppl.), 315–326.
Jenny, A. B. (1979). Commissural projections of the cortical hand motor area in monkeys. Journal of Comparative Neurology, 188, 137–146.
Jones, E. G. (1985). The thalamus. New York: Plenum.
Jones, E. G., Coulter, J. D., & Hendry, S. H. (1978). Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. Journal of Comparative Neurology, 181, 291–347.
Jones, E. G., Coulter, J. D., & Wise, S. P. (1979). Commissural columns in the sensory-motor cortex of monkeys. Journal of Comparative Neurology, 188, 113–136.
Jones, E. G., & Hendry, S. H. (1980). Distribution of callosal fibers around the hand representations in monkey somatic sensory cortex. Neuroscience Letters, 19, 167–172.
Killackey, H. P., Gould, H. J., Cusick, C. G., Pons, T. P., & Kaas, J. H. (1983). The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of New and Old World monkeys. Journal of Comparative Neurology, 219, 384–419.
Kuypers, H. G., & Brinkman, J. (1970). Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey. Brain Research, 24, 29–48.
Lemon, R. N., & Porter, R. (1976). Afferent input to movement-related precentral neurones in conscious monkeys. Proceedings of the Royal Society of London: Series B, 194, 313–339.
Logothetis, N. K., Paulis, J., Augath, M., Trinath, T., & Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150–157.
Ludman, C. N., Cooper, T. G., Ploutz-Synder, L. L., Potchen, E. J., & Meyer, R. A. (1996). Force of voluntary exercise does not affect sensorimotor cortex activation as detected by functional MRI at 1.5 T. NMR in Biomedicine, 9, 228–232.
Luppino, G., Matelli, M., Camarda, R., & Rizzolatti, G. (1993). Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. Journal of Comparative Neurology, 338, 114–140.
Menon, R. S. (2001). Imaging function in the working brain with fMRI. Current Opinion in Neurobiology, 11, 630–636.
Mima, T., Sadato, N., Yazawa, S., Hanakawa, T., Fukuyama, H., Yonekura, Y., & Shibasaki, H. (1999). Brain structures related to active and passive finger movements in man. Brain, 122, 1989–1997.
Muakkassa, K. F., & Strick, P. L. (1979). Frontal lobe inputs to primate motor cortex: Evidence for four somatotopically organized “premotor” areas. Brain Research, 177, 176–182.
Murray, E. A., & Coulter, J. D. (1981). Organization of corticospinal neurons in the monkey. Journal of Comparative Neurology, 195, 339–365.
Porro, C. A., Francescato, M. P., Cettolo, V., Diamond, M. E., Baraldi, P., Zuiani, C., Bassocchi, M., & di Prampero, P. E. (1996). Primary motor and sensory cortex activation during motor performance and motor imagery: A functional magnetic resonance imaging study. Journal of Neuroscience, 16, 7688–7698.
Prud’homme, M. J., Cohen, D. A., & Kalaska, J. F. (1994). Tactile activity in primate primary somatosensory cortex during active arm movements: Cytoarchitectonic distribution. Journal of Neurophysiology, 71, 173–181.
Raichle, M. E. (2000). The neural correlates of consciousness: An analysis of cognitive skill learning. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences (2nd ed., pp. 1313–1314). Cambridge, MA: MIT Press.
Rao, S. M., Binder, J. R., Bandettini, P. A., Hammeke, T. A., Yetkin, F. Z., Jesmanowicz, A., Lisk, L. M., Morris, G. L., Mueller, W. M., Estkowski, L. D., Wong, E. C., Haughton, V. M., & Hyde, J. S. (1993). Functional magnetic resonance imaging of complex human movements. Neurology, 43, 2311–2318.
Rausch, M., Spengler, F., & Eysel, U. T. (1998). Proprioception acts as the main source of input in human S-I activation experiments: A functional MRI study. NeuroReport, 9, 2865–2868.
Rouiller, E. M., Liang, F., Babalian, A., Moret, V., & Wiesendanger, M. (1994). Cerebellothalamocortical and pallidothalamocortical projections to the primary and supplementary motor cortical areas: A multiple tracing study in macaque monkeys. Journal of Comparative Neurology, 345, 185–213.
Sakai, S. T., Inase, M., & Tanji, J. (1996). Comparison of cerebellothalamic and pallidothalamic projections in the monkey (Macaca fuscata): A double anterograde labeling study. Journal of Comparative Neurology, 368, 215–228.
Schell, G. R., & Strick, P. L. (1984). The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. Journal of Neuroscience, 4, 539–560.
Soso, M. J., & Fetz, E. E. (1980). Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. Journal of Neurophysiology, 43, 1090–1110.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. Stuttgart: Thieme.
Tanji, J. (1994). The supplementary motor area in the cerebral cortex. Neuroscience Research, 19, 251–268.
Tanji, J., & Kurata, K. (1982). Comparison of movement-related activity in two cortical motor areas of primates. Journal of Neurophysiology, 48, 633–653.
Tanji, J., Okano, K., & Sato, K. (1988). Neuronal activity in cortical motor areas related to ipsilateral, contralateral and bilateral digit movements of the monkey. Journal of Neurophysiology, 60, 325–343.
Thickbroom, G. W., Phillips, B. A., Morris, I., Byrnes, M. L., & Mastaglia, F. L. (1998). Isometric force-related activity in sensorimotor cortex measured with functional MRI. Experimental Brain Research, 121, 59–64.
Thickbroom, G. W., Phillips, B. A., Morris, I., Byrnes, M. L., Sacco, P., & Mastaglia, F. L. (1999). Differences in functional magnetic resonance imaging of sensorimotor cortex during static and dynamic finger flexion. Experimental Brain Research, 126, 431–438.
Turner, R. S., Grafton, S. T., Votaw, J. R., DeLong, M. R., & Hoffmann, J. M. (1998). Motor subcircuits mediating the control of movement velocity: A PET study. Journal of Neurophysiology, 80, 2161–2176.
Wannier, T. M., Maier, M. A., & Hepp-Reymond, M. C. (1991). Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. Journal of Neurophysiology, 65, 572–589.
Weiller, C., Juptner, M., Fellows, S., Rijntjes, M., Leonhardt, G., Kiebel, S., Muller, S., Diener, H. C., & Thilmann, A. F. (1996). Brain representations of active and passive movements. NeuroImage, 4, 105–110.
Xiong, J., Parsons, L. M., Gao, J. H., & Fox, P. T. (1999). Interregional connectivity to primary motor cortex revealed using MRI resting state images. Human Brain Mapping, 8, 151–156.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by the Department of Radiology at Michigan State University.
Rights and permissions
About this article
Cite this article
Bernard, R.A., Goran, D.A., Sakai, S.T. et al. Cortical activation during rhythmic hand movements performed under three types of control: An fMRI study. Cognitive, Affective, & Behavioral Neuroscience 2, 271–281 (2002). https://doi.org/10.3758/CABN.2.3.271
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/CABN.2.3.271