The effect of leisure activity golf practice on motor imagery: an fMRI study in middle adulthood

Ladina Bezzola, Susan Mérillat, Lutz Jäncke, Ladina Bezzola, Susan Mérillat, Lutz Jäncke

Abstract

Much is known about practice-induced plasticity of the motor system. But it is not clear how a physical training influences the mental rehearsal of the practiced task and its associated hemodynamic responses. In the present longitudinal study with two measurement time-points, we used the method of functional magnetic resonance imaging (fMRI) and a motor imagery task, in order to explore the dynamic neuro-functional changes induced by a highly complex physical training. The 11 golf novices between the age of 40 and 60 years practiced the motor training as leisure activity. Additionally, data from an age and sex-matched control group without golf training was collected. As a main result, we demonstrate that changes between the two measurement time-points were only found in the golf novice group. The golf novices showed a decrease in hemodynamic responses during the mental rehearsal of the golf swing in non-primary motor areas after the 40 h of golf practice. Thus, the results indicate that a complex physical leisure activity induces functional neuroplasticity in the seldom studied population of middle-aged adults, and that this effect is evident during mental rehearsal of the practiced task. This finding supports the idea that (a) a skill improvement is associated with a modified activation pattern in the associated neuronal network that can be identified during mental rehearsal of the practiced task, and that (b) a strict training protocol is not necessary to induce functional neuroplasticity.

Keywords: fMRI; functional neuroplasticity; middle adulthood; motor imagery; motor learning.

Figures

Figure 1
Figure 1
Increased hemodynamic response while mentally rehearsing a golf swing (MI) in the golf and control group at baseline (T1). (1) left premotor cortex; (2) left superior parietal lobe; (3) left nucleus caudatus; (4) right premotor cortex; (5) right nucleus caudatus. The color bar represents the T-values.
Figure 2
Figure 2
Training-induced changes of neuronal recruitment while mentally rehearsing a golf swing (MI). (1), (2), (3) right premotor cortex; (4) left premotor cortex. The color bar represents the T-values. The indices relate to the numbers used in Table 4 and Figure 3.
Figure 3
Figure 3
Interaction effects for changes of neuronal recruitment during MI, between the golf (black) and the control (gray) group: dPMC, dorsal premotor cortex. The indices relate to the numbers used in Table 4 and Figure 2. Error bars represent 1 SE.

References

    1. Annett M. (1970). The contribution of the insula to motor aspects of speech production: a review and a hypothesis. Brain Lang. 89, 320–328 10.1016/S0093-934X(03)00347-X
    1. Bernstein N. (1967). The Coordination and Regulation of Movements. London: Pergamon Press
    1. Bezzola L., Merillat S., Gaser C., Jancke L. (2011). Training-induced neural plasticity in golf novices. J. Neurosci. 31, 12444–12448 10.1523/JNEUROSCI.1996-11.2011
    1. Debaere F., Wenderoth N., Sunaert S., Van Hecke P., Swinnen S. P. (2004). Changes in brain activation during the acquisition of a new bimanual coodination task. Neuropsychologia 42, 855–867 10.1016/j.neuropsychologia.2003.12.010
    1. Doyon J., Bellec P., Amsel R., Penhune V., Monchi O., Carrier J., Lehericy S., Benali H. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61–75 10.1016/j.bbr.2008.11.012
    1. Doyon J., Benali H. (2005). Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 15, 161–167 10.1016/j.conb.2005.03.004
    1. Draganski B., May A. (2008). Training-induced structural changes in the adult human brain. Behav. Brain Res. 192, 137–142 10.1016/j.bbr.2008.02.015
    1. Fourkas A. D., Bonavolonta V., Avenanti A., Aglioti S. M. (2008). Kinesthetic imagery and tool-specific modulation of corticospinal representations in expert tennis players. Cereb. Cortex 18, 2382–2390 10.1093/cercor/bhn005
    1. Gerardin E., Sirigu A., Lehericy S., Poline J. B., Gaymard B., Marsault C., Agid Y., Le Bihan D. (2000). Partially overlapping neural networks for real and imagined hand movements. Cereb. Cortex 10, 1093–1104 10.1093/cercor/10.11.1093
    1. Godde B., Voelcker-Rehage C. (2010). More automation and less cognitive control of imagined walking movements in high- versus low-fit older adults. Front. Aging Neurosci. 2:139 10.3389/fnagi.2010.00139
    1. Granert O., Peller M., Gaser C., Groppa S., Hallett M., Knutzen A., Deuschl G., Zeuner K. E., Siebner H. R. (2011). Manual activity shapes structure and function in contralateral human motor hand area. Neuroimage 54, 32–41 10.1016/j.neuroimage.2010.08.013
    1. Guillot A., Collet C., Nguyen V. A., Malouin F., Richards C., Doyon J. (2008). Functional neuroanatomical networks associated with expertise in motor imagery. Neuroimage 41, 1471–1483 10.1016/j.neuroimage.2008.03.042
    1. Halsband U., Lange R. K. (2006). Motor learning in man: a review of functional and clinical studies. J. Physiol. Paris 99, 414–424 10.1016/j.jphysparis.2006.03.007
    1. Hlustik P., Solodkin A., Noll D. C., Small S. L. (2004). Cortical plasticity during three-week motor skill learning. J. Clin. Neurophysiol. 21, 180–191
    1. Ilg R., Wohlschlager A. M., Gaser C., Liebau Y., Dauner R., Woller A., Zimmer C., Zihl J., Muhlau M. (2008). Gray matter increase induced by practice correlates with task-specific activation: a combined functional and morphometric magnetic resonance imaging study. J. Neurosci. 28, 4210–4215 10.1523/JNEUROSCI.5722-07.2008
    1. Ionta S., Ferretti A., Merla A., Tartaro A., Romani G. L. (2010). Step-by-step: the effects of physical practice on the neural correlates of locomotion imagery revealed by fMRI. Hum. Brain Mapp. 31, 694–702 10.1002/hbm.20898
    1. Jancke L. (2009). The plastic human brain. Restor. Neurol. Neurosci. 27, 521–538 10.3233/RNN-2009-0519
    1. Jancke L., Kleinschmidt A., Mirzazade S., Shah N. J., Freund H. J. (2001). The role of the inferior parietal cortex in linking the tactile perception and manual construction of object shapes. Cereb. Cortex 11, 114–121 10.1093/cercor/11.2.114
    1. Jancke L., Shah N. J., Peters M. (2000). Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Brain Res. Cogn. Brain Res. 10, 177–183 10.1016/S0926-6410(00)00028-8
    1. Jeannerod M. (2001). Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14, S103–S109 10.1006/nimg.2001.0832
    1. Karni A., Meyer G., Jezzard P., Adams M. M., Turner R., Ungerleider L. G. (1995). Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 10.1038/377155a0
    1. Koeneke S., Lutz K., Esslen M., Jancke L. (2006). How finger tapping practice enhances efficiency of motor control. Neuroreport 17, 1565–1569 10.1097/01.wnr.0000234748.80936.1d
    1. Koeneke S., Lutz K., Wustenberg T., Jancke L. (2004). Long-term training affects cerebellar processing in skilled keyboard players. Neuroreport 15, 1279–1282
    1. Lacourse M. G., Orr E. L., Cramer S. C., Cohen M. J. (2005). Brain activation during execution and motor imagery of novel and skilled sequential hand movements. Neuroimage 27, 505–519 10.1016/j.neuroimage.2005.04.025
    1. Lotze M., Halsband U. (2006). Motor imagery. J. Physiol. Paris 99, 386–395 10.1016/j.jphysparis.2006.03.012
    1. Lustig C., Shah P., Seidler R., Reuter-Lorenz P. A. (2009). Aging, training, and the brain: a review and future directions. Neuropsychol. Rev. 19, 504–522 10.1007/s11065-009-9119-9
    1. Ma L., Wang B., Narayana S., Hazeltine E., Chen X., Robin D. A., Fox P. T., Xiong J. (2010). Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning. Brain Res. 1318, 64–76 10.1016/j.brainres.2009.12.073
    1. Milton J., Small S. L., Solodkin A. (2008). Imaging motor imagery: methodological issues related to expertise. Methods 45, 336–341 10.1016/j.ymeth.2008.05.002
    1. Milton J., Solodkin A., Hlustik P., Small S. L. (2007). The mind of expert motor performance is cool and focused. Neuroimage 35, 804–813 10.1016/j.neuroimage.2007.01.003
    1. Olsson C. J., Jonsson B., Larsson A., Nyberg L. (2008a). Motor representations and practice affect brain systems underlying imagery: an fMRI study of internal imagery in novices and active high jumpers. Open Neuroimag. J. 2, 5–13 10.2174/1874440000802010005
    1. Olsson C. J., Jonsson B., Nyberg L. (2008b). Learning by doing and learning by thinking: an fMRI study of combining motor and mental training. Front. Hum. Neurosci. 2:5 10.3389/neuro.09.005.2008
    1. Page S. J., Szaflarski J. P., Eliassen J. C., Pan H., Cramer S. C. (2009). Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil. Neural Repair 23, 382–388 10.1177/1545968308326427
    1. Pascual-Leone A., Amedi A., Fregni F., Merabet L. B. (2005). The plastic human brain cortex. Annu. Rev. Neurosci. 28, 377–401 10.1146/annurev.neuro.27.070203.144216
    1. Ross J. S., Tkach J., Ruggieri P. M., Lieber M., Lapresto E. (2003). The mind's eye: functional MR imaging evaluation of golf motor imagery. AJNR Am. J. Neuroradiol. 24, 1036–1044
    1. Rovio S., Kareholt I., Helkala E. L., Viitanen M., Winblad B., Tuomilehto J., Soininen H., Nissinen A., Kivipelto M. (2005). Leisure-time physical activity at midlife and the risk of dementia and Alzheimer's disease. Lancet Neurol. 4, 705–711 10.1016/S1474-4422(05)70198-8
    1. Seidler R. D. (2007). Older adults can learn to learn new motor skills. Behav. Brain Res. 183, 118–122 10.1016/j.bbr.2007.05.024
    1. Serrien D. J., Ivry R. B., Swinnen S. P. (2006). Dynamics of hemispheric specialization and integration in the context of motor control. Nat. Rev. Neurosci. 7, 160–166 10.1038/nrn1849
    1. Solodkin A., Hlustik P., Chen E. E., Small S. L. (2004). Fine modulation in network activation during motor execution and motor imagery. Cereb. Cortex 14, 1246–1255 10.1093/cercor/bhh086
    1. Studer B., Koeneke S., Blum J., Jancke L. (2010). The effects of practice distribution upon the regional oscillatory activity in visuomotor learning. Behav. Brain Funct. 6, 8 10.1186/1744-9081-6-8
    1. Szameitat A. J., Shen S., Sterr A. (2007). Motor imagery of complex everyday movements. An fMRI study. Neuroimage 34, 702–713 10.1016/j.neuroimage.2006.09.033
    1. Tuller B., Turvey M. T., Fitch H. L. (1982). “The Bernstein perspective. II. The concept of muscle linkage or coordinative structure,” in Human Motor Behavior, ed Kelso. J. A. S. (Hillsdale, NJ, London: Lawrence Erlbaum Associates; ), 239–252
    1. Ungerleider L. G., Doyon J., Karni A. (2002). Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 78, 553–564 10.1006/nlme.2002.4091
    1. Verghese J., Lipton R. B., Katz M. J., Hall C. B., Derby C. A., Kuslansky G., Ambrose A. F., Sliwinski M., Buschke H. (2003). Leisure activities and the risk of dementia in the elderly. N. Engl. J. Med. 348, 2508–2516 10.1056/NEJMoa022252
    1. Verwey W. B. (2010). Diminished motor skill development in elderly: indications for limited motor chunk use. Acta Psychol. (Amst.) 134, 206–214 10.1016/j.actpsy.2010.02.001
    1. Verwey W. B., Abrahamse E. L., Ruitenberg M. F., Jimenez L., De Kleine E. (2011). Motor skill learning in the middle-aged: limited development of motor chunks and explicit sequence knowledge. Psychol. Res. 75, 406–422 10.1007/s00426-011-0320-0

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe