Experimental Brain Research

, Volume 208, Issue 2, pp 189–201 | Cite as

Premovement brain activity in a bimanual load-lifting task

  • Tommy H. B. Ng
  • Paul F. Sowman
  • Jon Brock
  • Blake W. Johnson
Research Article

Abstract

Even the simplest volitional movements must be precisely coordinated with anticipatory postural adjustments. Little is currently known about the neural networks that coordinate these adjustments in healthy adults. We measured brain activity prior to movement during a bimanual load-lifting task, designed to elicit anticipatory adjustments in a restricted and well-defined set of musculature in the arm. Electroencephalography and magnetoencephalography brain measurements were obtained from eleven participants while they performed a bimanual load-lifting task that required precise inter-limb coordination. Anticipatory biceps brachii inhibition in the loaded arm was associated with a robust desynchronization of the beta rhythm. Beamforming analyses localized beta band responses to the parietal lobules, pre- and post-central gyri, middle and medial frontal gyri, basal ganglia and thalamus. The current study shows that premovement brain activity in a bimanual load-lifting task can be imaged with magnetoencephalography. Future experiments will partition out brain activity associated with anticipatory postural adjustments and volitional movements. The experimental paradigm will also be useful in the study of motor function in patients with developmental or degenerative disorders.

Keywords

Anticipatory postural adjustments Beamforming Bimanual load-lifting task Event-related desynchronization Magnetoencephalography Motor coordination 

Notes

Acknowledgments

The authors gratefully acknowledge the collaboration of Kanazawa Institute of Technology and Yokogawa Electric Corporation in establishing the KIT-Macquarie MEG laboratory. We thank Dr. Graciela Tesan and Ms. Melanie Reid for technical assistance and Dr. Thomas Nichols, Dr. Mark Williams, and Dr. Vladimir Litvak for helpful advice regarding SPM analysis.

Conflict of interest

The authors report no conflict of interest.

References

  1. Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271CrossRefPubMedGoogle Scholar
  2. Alexander GE, Crutcher MD, Delong MR (1990) Basal ganglia thalamo-cortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146CrossRefPubMedGoogle Scholar
  3. Almeida QJ, Wishart LR, Lee TD (2002) Bimanual coordination deficits with Parkinson’s disease: the influence of movement speed and external cueing. Mov Disord 17:30–37CrossRefPubMedGoogle Scholar
  4. Andersen RA, Snyder LH, Bradley DC, Xing J (1997) Multimodal representation of space in the posterior parietal cortex and its use in planning movement. Annu Rev Neurosci 20:303–330CrossRefPubMedGoogle Scholar
  5. Babin-Ratte S, Sirigu A, Gilles M, Wing A (1999) Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration. Exp Brain Res 128:81–85CrossRefPubMedGoogle Scholar
  6. Ball T, Schreiber A, Feige B, Wagner M, Lucking CH, Kristeva-Feige R (1999) The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 10:682–694CrossRefPubMedGoogle Scholar
  7. Beiser DG, Hua SE, Houk JC (1997) Network models of the basal ganglia. Curr Opin Neurobiol 7:185–190CrossRefPubMedGoogle Scholar
  8. Benvenuti F, Stanhope SJ, Thomas SL, Panzer VP, Hallet M (1997) Flexibility of anticipatory postural adjustments revealed by self-paced and reaction-time arm movements. Brain Res 7:59–70CrossRefGoogle Scholar
  9. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund HJ (1999a) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI study. Eur J Neurosci 11:3276–3286CrossRefPubMedGoogle Scholar
  10. Binkofski F, Buccino G, Stephan KM, Rizzolatti G, Seitz RJ, Freund HJ (1999b) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res 128:210–213CrossRefPubMedGoogle Scholar
  11. Brinkman C (1981) Lesions in supplementary motor area interfere with a monkey’s performance of a bimanual coordination task. Neurosci Lett 27:267–270CrossRefPubMedGoogle Scholar
  12. Brinkman C (1984) Supplementary motor area of the monkey’s cerebral cortex: short- and long term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4:918–929PubMedGoogle Scholar
  13. Brooks DJ (1995) The role of basal ganglia in motor control: contributions from PET. J Neurol Sci 128:1–13CrossRefPubMedGoogle Scholar
  14. Cheyne D, Bakhtazad L, Gaetz W (2006) Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event-related beamforming approach. Hum Brain Mapp 27:213–229CrossRefPubMedGoogle Scholar
  15. Cheyne D, Bells S, Ferrari P, Gaetz W, Bostan AC (2008) Self-paced movements induce high-frequency gamma oscillations in primary motor cortex. Neuroimage 42:332–342CrossRefPubMedGoogle Scholar
  16. Cochin S, Barthelemy C, Roux S, Martineau J (2001) Electroencephalographic activity during perception of motion in childhood. Eur J Neurosci 13:1791–1796CrossRefPubMedGoogle Scholar
  17. Colebatch JG, Deiber MP, Passingham RE, Friston KJ, Frackowiak RS (1991) Regional cerebral blood flow during voluntary arm and hand movements in human subjects. J Neurophysiol 65:1392–1401PubMedGoogle Scholar
  18. Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movements in humans. J Physiol (Lond) 437:635–653Google Scholar
  19. Derambure P, Defebvre L, Dujardin K, Bourriez JL, Jacquesson JM, Destee A, Guieu JD (1993) Effect of aging on the spatio-temporal pattern of event-related desynchronization during voluntary movement. Electroencephalogr Clin Neurophysiol 89:197–203CrossRefPubMedGoogle Scholar
  20. DeVito JL, Anderson ME (1982) An autoradiographic study of efferent connections of the globus in Macaca mulatta. Exp Brain Res 46:107–117CrossRefPubMedGoogle Scholar
  21. Diedrichsen J, Verstynen T, Lehman SL, Ivry RB (2005) Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93:801–812CrossRefPubMedGoogle Scholar
  22. Diener HC, Dichgans J, Guschlbauer B, Bacher M, Langenbach P (1989) Disturbances of motor preparation in basal ganglia and cerebellar disorders. Prog Brain Res 80:481–488CrossRefPubMedGoogle Scholar
  23. DiFabio RP (1987) Reliability of computerized surface electromyography for determining the onset of muscle activity. Phys Ther 67:43–48Google Scholar
  24. Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667–689PubMedGoogle Scholar
  25. Forget R, Lamarre Y (1990) Anticipatory postural adjustment in the absence of normal peripheral feedback. Brain Res 508:176–179CrossRefPubMedGoogle Scholar
  26. Fujioka T, Zendel BR, Ross B (2010) Endogenous neuromagnetic activity for mental hierarchy of timing. J Neurosci 30:3458–3466CrossRefPubMedGoogle Scholar
  27. Green JJ, McDonald JJ (2008) Electrical neuroimaging reveals timing of attentional control activity in human brain. PLoS Biol 6:730–738CrossRefGoogle Scholar
  28. Gurfinkel VS, Lipshits MI, Lestienne FG (1988) Anticipatory neck muscle activity associated with rapid arm muscles. Neurosci Lett 94:104–108CrossRefPubMedGoogle Scholar
  29. He SQ, Dum RP, Strick PL (1995) Topographic organization of cortico-spinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci 15:3284–3306PubMedGoogle Scholar
  30. Hirashima M, Kadota H, Sakurai S, Kudo K, Ohtsuki T (2002) Sequential muscle activity and its functional role in the upper extremity and trunk during overarm throwing. J Sports Sci 20:301–310CrossRefPubMedGoogle Scholar
  31. Hugon M, Massion J, Wiesendanger M (1982) Anticipatory postural changes induced by active unloading and comparison with passive unloading in man. Eur J Physiol 393:292–296CrossRefGoogle Scholar
  32. Illinsky IA, Jouandet ML, Goldman-Rakic PS (1985) Organization of the nigrothalamocortical system in the rhesus monkey. J Comp Neurol 236:315–330CrossRefGoogle Scholar
  33. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Puetz B, Yoshoka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403:192–195CrossRefPubMedGoogle Scholar
  34. Ioffe M, Massion J, Gantchev N, Dufosse M, Kulikov MA (1996) Coordination between posture and movement in a bimanual load-lifting task: is there a transfer? Exp Brain Res 109:450–456CrossRefPubMedGoogle Scholar
  35. Ivry RB, Keele SW, Diener HC (1988) Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res 73:167–180CrossRefPubMedGoogle Scholar
  36. Janke L, Kleinschmidt A, Mirazazade S, Shah NJ, Freund HJ (2001) The role of the inferior parietal cortex in linking the tactile perception and manual construction of object shapes. Cereb Cortex 11:114–121CrossRefGoogle Scholar
  37. Johnson TN, Rosvold HE (1971) Topographic projections on the globus pallidus and the substantia nigra of selectively placed lesions in the precommissural caudate nucleus and putamen in the monkey. Exp Neurol 33:584–596CrossRefPubMedGoogle Scholar
  38. Johnson KA, Cunnington R, Bradshaw JL, Phillips JG, Iansek R, Rogers MA (1998) Bimanual coordination in Parkinson’s disease. Brain 121:743–753CrossRefPubMedGoogle Scholar
  39. Jueptner M, Weiller C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121:1437–1449CrossRefPubMedGoogle Scholar
  40. Kado H, Higuchi M, Shimogawara M, Haruta Y, Adachi Y, Kawai J, Ogata H, Uehara G (1999) Magnetoencephalogram system developed at KIT. IEEE T Appl Supercon 9:4057–4062CrossRefGoogle Scholar
  41. Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727CrossRefPubMedGoogle Scholar
  42. Kim SG, Richter W, Ugurbil K (1997) Limitations of temporal resolution in functional MRI. Magnet Reson Med 37:631–636CrossRefGoogle Scholar
  43. Kropotov JD, Etlinger SC (1999) Selection of actions in the basal ganglia-thalamocortical circuits: review and model. Int J Psychophysiol 31:197–217CrossRefPubMedGoogle Scholar
  44. Lacquaniti F, Maioli C (1989) The role of preparation in tuning anticipatory and reflex responses during catching. J Neurosci 9:134–148PubMedGoogle Scholar
  45. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131CrossRefPubMedGoogle Scholar
  46. Laplane D, Talairach J, Meininger V, Bancaud J, Orgogozo JM (1977) Clinical consequences of corticectomies involving supplementary motor area in man. J Neurol Sci 43:301–314CrossRefGoogle Scholar
  47. Lee KM, Chang KH, Roh JK (1999) Subregions within the supplementary motor area activated at different stages of movement preparation and execution. Neuroimage 9:117–123CrossRefPubMedGoogle Scholar
  48. Macpherson J, Wiesendanger M, Marangoz C, Miles TS (1982) Corticospinal neurones of the supplementary motor area of monkeys. Exp Brain Res 48:81–88CrossRefPubMedGoogle Scholar
  49. Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21:450–455CrossRefPubMedGoogle Scholar
  50. Martineau J, Schmitz C, Assaiante C, Blanc R, Barthelemy C (2004) Impairment of a cortical related desynchronisation during a bimanual load-lifting task in children with autistic disorder. Neurosci Lett 367:298–303CrossRefPubMedGoogle Scholar
  51. Mason CR, Gomez JE, Ebner TJ (2001) Hand synergies during reach-to-grasp. J Neurophysiol 86:2896–2910PubMedGoogle Scholar
  52. McFadyen B, Malouin F, Dumas F (2001) Anticipatory locomotor control for obstacle avoidance in mid-childhood aged children. Gait Posture 13:7–16CrossRefPubMedGoogle Scholar
  53. Morton SM, Lang CE, Bastian AJ (2001) Inter- and intra-limb generalization of adaptation during catching. Exp Brain Res 141:438–445CrossRefPubMedGoogle Scholar
  54. Muller F, Dichgans J (1994) Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions. Exp Brain Res 101:485–492CrossRefPubMedGoogle Scholar
  55. Nowak DA, Hermsdorfer J, Marquardt C, Fuchs HH (2002) Grip and load force coupling during discrete vertical arm movements with a grasped object in cerebellar atrophy. Exp Brain Res 145:28–39CrossRefPubMedGoogle Scholar
  56. Nunez PL, Westdorp AF (1994) The surface laplacian, high resolution EEG and controversies. Brain Topogr 6:221–226CrossRefPubMedGoogle Scholar
  57. Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872CrossRefPubMedGoogle Scholar
  58. Parent A, Bouchard C, Smith Y (1984) The striatopallidal and striatonigral projections: two distinct fiber systems in primate. Brain Res 303:385–390CrossRefPubMedGoogle Scholar
  59. Pfurtscheller G, Aranibar A (1979) Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalogr Clin Neurophysiol 46:138–146CrossRefPubMedGoogle Scholar
  60. Pfurtscheller G, Berghold A (1989) Patterns of cortical activation during planning of voluntary movement. Electroencephalogr Clin Neurophysiol 72:250–258CrossRefPubMedGoogle Scholar
  61. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronisation and desynchronisation: basic principles. Clin Neurophysiol 110:1842–1857CrossRefPubMedGoogle Scholar
  62. Pfurtscheller G, Pregenzer M, Neuper C (1994) Visualization of the sensorimotor areas involved in preparation for hand movement based on classification of mu and beta rhythms in single EEG trials in man. Neurosci Lett 181:43–46CrossRefPubMedGoogle Scholar
  63. Pfurtscheller G, Graimann B, Huggins JE, Levine SP, Schuh LA (2003) Spatiotemporal patterns of beta desynchronisation and gamma synchronisation in corticographic data during self-paced movement. Clin Neurophysiol 114:1226–1236CrossRefPubMedGoogle Scholar
  64. Rushworth MF, Nixon PD, Passingham RE (1997) Parietal cortex and movement. I. Movement selection and reaching. Exp Brain Res 117:292–310CrossRefPubMedGoogle Scholar
  65. Sakai K, Hikosaka O, Miyauchi S, Takino R, Tamada T, Iwata NK, Nielsen M (1999) Neural representation of a rhythm depends on its interval ratio. J Neurosci 19:10074–10081PubMedGoogle Scholar
  66. Salmelin R, Hamalainen M, Kajola M, Hari R (1995) Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 2:237–243CrossRefPubMedGoogle Scholar
  67. Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560PubMedGoogle Scholar
  68. Schmitz C, Martin N, Assaiante C (2002) Building anticipatory postural adjustments during childhood: a kinematic and electromyographic analysis of unloading in children from 4 to 8 years of age. Exp Brain Res 142:354–364CrossRefPubMedGoogle Scholar
  69. Schmitz C, Martineau J, Barthelemy C, Assaiante C (2003) Motor control and children with autism: deficit of anticipatory function? Neurosci Lett 348:17–20CrossRefPubMedGoogle Scholar
  70. Schmitz C, Jenmalm P, Westling G, Ehrsson H, Forssberg H (2005) Anticipatory postural adjustments in a bimanual load-lifting task: central aspects. Gait Posture 21:S50CrossRefGoogle Scholar
  71. Schneiberg S, Sveistrup H, McFadyen B, McKinley P, Levin MF (2002) The development of coordination for reach-to-grasp movements in children. Exp Brain Res 146:142–154CrossRefPubMedGoogle Scholar
  72. Serrien DJ, Wiesendanger M (1999) Grip-load force coordination in cerebellar patients. Exp Brain Res 128:76–80CrossRefPubMedGoogle Scholar
  73. Stancak JA, Pfurtscheller G (1996) Event-related desynchronization of central beta rhythms in brisk and slow self-paced finger movements of dominant and nondominant hand. Cognitive Brain Res 4:171–184CrossRefGoogle Scholar
  74. Stoeckel MC, Weder B, Binkofski F, Buccino G, Shah NJ, Seitz RJ (2003) A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study. Neuroimage 9:1103–1114CrossRefGoogle Scholar
  75. Strick PL (1976) Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J Neurophysiol 39:1020–1031PubMedGoogle Scholar
  76. Szabo J (1967) Projections from the body of the caudate nucleus in the rhesus monkey. Exp Neurol 27:1–15CrossRefGoogle Scholar
  77. Taga G (1998) A model of the neuro-musculo-skeletal system for anticipatory adjustment of human locomotion during obstacle avoidance. Biol Cybern 78:9–17CrossRefPubMedGoogle Scholar
  78. Taniguchi M, Kato A, Fujita N, Hirata M, Tanaka H, Kihara T, Ninomiya H, Hirabuki N, Nakamura H, Robinson SE, Cheyne D, Yoshimine T (2000) Movement-related desynchronization of the cerebral cortex studied with spatially filtered magnetoencephalography. Neuroimage 12:298–306CrossRefPubMedGoogle Scholar
  79. Traub MM, Rothwell JC, Marsden CD (1980) Anticipatory postural reflexes in Parkinson’s disease and other akinetic-rigid syndromes and in cerebellar ataxia. Brain 103:393–412CrossRefPubMedGoogle Scholar
  80. Uehara G, Adachi Y, Kawai J, Shimogawara M, Higuchi M, Haruta Y, Ogata H, Kado H (2003) Multi-channel SQUID systems for biomagnetic measurement. IEICE T Electron E86-C(1):43–54Google Scholar
  81. Van Veen BD, Buckley KM (1988) Beamforming: a versatile approach to spatial filtering. IEEE T Acoust Speech 5:4–24Google Scholar
  82. Viallet F, Massion J, Massarino R, Khalil R (1987) Performance of a bimanual load-lifting task by Parkinsonian patients. J Neurol Neurosurg Psychiatry 50:1274–1283CrossRefPubMedGoogle Scholar
  83. Viallet F, Massion J, Massarino R, Khalil R (1992) Coordination between posture and movement in a bimanual load-lifting task: putative role of medial frontal region including the supplementary motor area. Exp Brain Res 88:674–684CrossRefPubMedGoogle Scholar
  84. Wexler BE, Fulbright RK, Lacadie CM, Skudlarski P, Kelz MB, Constable T, Gore JC (1997) An fMRI study of the human cortical motor system response to increasing functional demands. Magn Reson Imaging 15:385–396CrossRefPubMedGoogle Scholar
  85. Wiesendanger R, Wiesendanger M (1985) The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (macaca fascicularis). Exp Brain Res 59:91–104PubMedGoogle Scholar
  86. Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:313–321CrossRefGoogle Scholar
  87. Worsley KJ, Marret S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58–73CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Tommy H. B. Ng
    • 1
  • Paul F. Sowman
    • 1
  • Jon Brock
    • 1
  • Blake W. Johnson
    • 1
  1. 1.Macquarie Centre for Cognitive ScienceMacquarie UniversitySydneyAustralia

Personalised recommendations