Skip to main content
Log in

Neural mechanisms of movement speed and tau as revealed by magnetoencephalography

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

A fundamental aspect of goal-directed behavior concerns the closure of motion-gaps in a timely fashion. In this context, the critical variable is the time-to-closure, called tau (Lee in Perception 5:437–459, 1976), and is defined as the ratio of the current distance-to-goal gap over the current instantaneous speed towards the goal. In this study, we investigated the neural mechanisms of speed and tau in pointing hand movements by recording MEG activity from the whole brain of 20 right-handed healthy human subjects operating a joystick with their right hand. The relations between neural signals and speed and tau were analyzed using an autoregressive multiple regression model, where the time-varying MEG signal was the dependent variable and the corresponding value of speed and tau were the independent variables. With respect to speed, we found that 81% of sensors showed significant relations over the left frontal-parietal, left parieto-temporal, and, less prominently, the right temporo-occipital sensor space. These results document the widespread involvement of brain areas with movement speed, especially in the left hemisphere (i.e., contralateral to the moving limb), in accord with previous studies. With respect to tau, 22% of sensors showed significant relations over the parietal (bilaterally), right parietal-temporal, and, less prominently, the left temporo-occipital sensor space. The tau effects often occurred concurrently with speed effects and spatially overlapped in the left fronto-parietal sensors. These findings document for the first time the time-varying, dynamic processing of information regarding tau in specific brain areas, including the right parietal cortex. This is of special interest, for that area has been found to be involved in processing information concerning the duration of time intervals in perceptual tasks (Harrington et al. in J Neurosci 18:1085–1095, 1998; Rao et al. in Nat Neurosci 4:317–323, 2001). Since tau is itself a time interval, we hypothesize that the right parietal focus of tau processing observed in this study reflects the ongoing processing of tau as an interval for a timely arrival of the hand to the target.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ashe J, Georgopoulos AP (1994) Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex 4:590–600

    Article  PubMed  CAS  Google Scholar 

  • Assmus A, Marshall JC, Ritzl A, Noth J, Zilles K, Fink GR (2003) Left inferior parietal cortex integrates time and space during collision judgments. NeuroImage 20(Suppl 1):S82–S88

    Article  PubMed  Google Scholar 

  • Atkeson C, Hollerbach J (1985) Kinematic features of unrestrained vertical arm movements. J Neurosci 5:2318–2330

    PubMed  CAS  Google Scholar 

  • Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2005) Parietal representation of hand velocity in a copy task. J Neurophysiol 93:508–518

    Article  PubMed  Google Scholar 

  • Baillet S, Mosher JC, Leahy RM (2001) Electromagnetic brain mapping. Signal Process Mag IEEE 18:14–30

    Article  Google Scholar 

  • Basso G, Nichelli P, Frassinetti F, di Pellegrino G (1996) Time perception in a neglected space. NeuroReport 7:2111–2114

    Article  PubMed  CAS  Google Scholar 

  • Bastiaansen MC, Knösche TR (2000) Tangential derivative mapping of axial MEG applied to event-related desynchronization research. Clin Neurophysiol 111:1300–1305

    Article  PubMed  CAS  Google Scholar 

  • Battaglia-Mayer A, Caminiti R (2002) Optic ataxia as a result of the breakdown of the global tuning fields of parietal neurones. Brain 125:225–237

    Article  PubMed  Google Scholar 

  • Battaglia-Mayer A, Caminiti R, Lacquaniti F, Zago M (2003) Multiple levels of representation of reaching in the parieto-frontal network. Cereb Cortex 13:1009–1022

    Article  PubMed  Google Scholar 

  • Battaglia-Mayer A, Archambault PS, Caminiti R (2006) The cortical network for eye-hand coordination and its relevance to understanding motor disorders of parietal patients. Neuropsychologia 44:2607–2620

    Article  PubMed  Google Scholar 

  • Battelli L, Pascual-Leone A, Cavanagh P (2007) The ‘when’ pathway of the right parietal lobe. Trends Cogn Sci 11:204–210

    Article  PubMed  Google Scholar 

  • Becchio C, Bertone C (2006) Time and neglect: abnormal temporal dynamics in unilateral spatial neglect. Neuropsychologia 44:2775–2782

    Article  PubMed  Google Scholar 

  • Beggs WDA, Howarth CI (1972) The movement of the hand towards a target. Q J Exp Psychol 24:448–453

    Article  PubMed  CAS  Google Scholar 

  • Blaschke T, Wiskott L (2004) CuBICA: independent component analysis by simultaneous third- and fourth-order cumulant diagonalization. IEEE Trans Signal Process 52:1250–1256

    Article  Google Scholar 

  • Boline J, Ashe J (2005) On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional dynamic isometric force. Exp Brain Res 167:148–159

    Article  PubMed  Google Scholar 

  • Bosch V (2000) Statistical analysis of multi-subject fMRI data: assessment of focal activations. J Magn Reson Imaging 11:61–64

    Article  PubMed  CAS  Google Scholar 

  • Box GEP, Hunter WG, Hunter JS (1978) Statistics for experimenters: an introduction to design, data analysis, and model building. Wiley, New York

    Google Scholar 

  • Buneo CA, Andersen RA (2006) The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44:2594–2606

    Article  PubMed  Google Scholar 

  • Chafee MV, Goldman-Rakic PS (1998) Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79:2919–2940

    PubMed  CAS  Google Scholar 

  • Chafee MV, Goldman-Rakic PS (2000) Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. J Neurophysiol 83:1550–1566

    PubMed  CAS  Google Scholar 

  • Craig CM, Lee DN (1999) Neonatal control of nutritive sucking pressure: evidence for an intrinsic tau-guide. Exp Brain Res 124:371–382

    Article  PubMed  CAS  Google Scholar 

  • Craig CM, Lee DN, Freer YN, Laing IA (1999) Modulations in breathing patterns during intermittent feeding in term infants and preterm infants with bronchopulmonary dysplasia. Dev Med Child Neurol 41:616–624

    Article  PubMed  CAS  Google Scholar 

  • Craig CM, Delay D, Grealy MA, Lee DN (2000a) Guiding the swing in golf putting. Nature 405:295–296

    Article  PubMed  CAS  Google Scholar 

  • Craig CM, Grealy MA, Lee DN (2000b) Detecting motor abnormalities in preterm infants. Exp Brain Res 131:359–365

    Article  PubMed  CAS  Google Scholar 

  • Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2:563–567

    Article  PubMed  CAS  Google Scholar 

  • Field DT, Wann JP (2005) Perceiving time to collision activates the sensorimotor cortex. Curr Biol 15:453–458

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17:1519–1528

    PubMed  CAS  Google Scholar 

  • Fu QG, Suarez JI, Ebner TJ (1993) Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. J Neurophysiol 70:2097–2116

    PubMed  CAS  Google Scholar 

  • Fu QG, Flament D, Coltz JD, Ebner TJ (1995) Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol 73:836–854

    PubMed  CAS  Google Scholar 

  • Genovesio A, Tsujimoto S, Wise SP (2006) Neuronal activity related to elapsed time in prefrontal cortex. J Neurophysiol 95:3281–3285

    Article  PubMed  Google Scholar 

  • Georgopoulos AP (2007) A tribute to tau. In: Pepping G-J, Grealy MA (eds) Closing the gap the scientific writings of David N. Lee. Lawrence Erlbaum Assoc Inc., NJ, pp 157–161

    Google Scholar 

  • Graziano MS, Cooke DF (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44:2621–2635

    Article  PubMed  Google Scholar 

  • Grea H, Pisella L, Rossetti Y, Desmurget M, Tilikete C, Grafton S, Prablanc C, Vighetto A (2002) A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements. Neuropsychologia 40:2471–2480

    Article  PubMed  Google Scholar 

  • Grefkes C, Ritzl A, Zilles K, Fink GR (2004) Human medial intraparietal cortex subserves visuomotor coordinate transformation. NeuroImage 23:1494–1506

    Article  PubMed  Google Scholar 

  • Harrington DL, Haaland KY, Knight RT (1998) Cortical networks underlying mechanisms of time perception. J Neurosci 18:1085–1095

    PubMed  CAS  Google Scholar 

  • Harrington DL, Boyd LA, Mayer AR, Sheltraw DM, Lee RR, Huang M, Rao SM (2004) Neural representation of interval encoding and decision making. Cogn Brain Res 21:193–205

    Article  Google Scholar 

  • Hillebrand A, Barnes GR (2002) A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. NeuroImage 16:638–650

    Article  PubMed  CAS  Google Scholar 

  • Hoshi E (2006) Functional specialization within the dorsolateral prefrontal cortex: a review of anatomical and physiological studies of non-human primates. Neurosci Res 54:73–84

    Article  PubMed  Google Scholar 

  • Hoshi E, Tanji J (2004) Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. J Neurophysiol 92:3482–3499

    Article  PubMed  Google Scholar 

  • Hoshi E, Shima K, Tanji J (2000) Neuronal activity in the primate prefrontal cortex in the process of motor selection based on two behavioral rules. J Neurophysiol 83:2355–2373

    PubMed  CAS  Google Scholar 

  • Husain M, Shapiro K, Martin J, Kennard C (1997) Abnormal temporal dynamics of visual attention in spatial neglect patients. Nature 385:154–156

    Article  PubMed  CAS  Google Scholar 

  • Ioannides AA (2001) Real time human brain function: observations and inferences from single trial analysis of magnetoencephalographic signals. Clin Electroencephalogr 32:98–111

    PubMed  CAS  Google Scholar 

  • Ioannides AA (2006) Magnetoencephalography as a research tool in neuroscience: state of the art. Neuroscientist 12:524–544

    Article  PubMed  Google Scholar 

  • Janssen P, Shadlen MN (2005) A representation of the hazard rate of elapsed time in macaque area LIP. Nat Neurosci 8:234–241

    Article  PubMed  CAS  Google Scholar 

  • Jerbi K, Lachaux JP, N’Diaye K, Pantazis D, Leahy RM, Garnero L, Baillet S (2007) Coherent neural representation of hand speed in humans revealed by MEG imaging. Proc Natl Acad Sci USA 104:7676–7681

    Article  PubMed  CAS  Google Scholar 

  • Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102–119

    Article  PubMed  CAS  Google Scholar 

  • Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 4:1020–1025

    Article  PubMed  CAS  Google Scholar 

  • Karjalainen PA, Kaipio JP, Koistinen AS, Vauhkonen M (1999) Subspace regularization method for the single-trial estimation of evoked potentials. IEEE Trans Biomed Eng 46:849–860

    Article  PubMed  CAS  Google Scholar 

  • Kelso JA, Fuchs A, Lancaster R, Holroyd T, Cheyne D, Weinberg H (1998) Dynamic cortical activity in the human brain reveals motor equivalence. Nature 392:814–818

    Article  PubMed  CAS  Google Scholar 

  • Langheim FJ, Leuthold AC, Georgopoulos AP (2006) Synchronous dynamic brain networks revealed by magnetoencephalography. Proc Natl Acad Sci USA 103:455–459

    Article  PubMed  CAS  Google Scholar 

  • Lee DN (1976) A theory of visual control of braking based on information about time-to-collision. Perception 5:437–459

    Article  PubMed  CAS  Google Scholar 

  • Lee DN (1998) Guiding movement by coupling Taus. Ecol Psychol 10:221–250

    Article  Google Scholar 

  • Lee DN, Reddish PE (1981) Plummeting gannets: a paradigm of ecological optics. Nature 293:293–294

    Article  Google Scholar 

  • Lee DN, van der Weel FR, Hitchcock T, Matejowsky E, Pettigrew JD (1992) Common principle of guidance by echolocation and vision. J Comp Physiol [A] 171:563–571

    CAS  Google Scholar 

  • Lee DN, Simmons JA, Saillant PA, Bouffard F (1995) Steering by echolocation: a paradigm of ecological acoustics. J Comp Physiol [A] 176:347–354

    CAS  Google Scholar 

  • Lee DN, Craig CM, Grealy MA (1999) Sensory and intrinsic coordination of movement. Proc Biol Sci 266:2029–2035

    Article  PubMed  CAS  Google Scholar 

  • Lee DN, Georgopoulos AP, Clark MJ, Craig CM, Port NL (2001) Guiding contact by coupling the taus of gaps. Exp Brain Res 139:151–159

    Article  PubMed  CAS  Google Scholar 

  • Leon MI, Shadlen MN (2003) Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38:317–327

    Article  PubMed  CAS  Google Scholar 

  • Leuthold AC (2003) Subtraction of heart artifact from MEG data: the matched filter revisited. Soc Neurosci Abstr 863:15

    Google Scholar 

  • Liu L, Ioannides AA (1996) A correlation study of averaged and single trial MEG signals: the average describes multiple histories each in a different set of single trials. Brain Topogr 8:385–396

    Article  PubMed  CAS  Google Scholar 

  • 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. J Comp Neurol 338:114–140

    Article  PubMed  CAS  Google Scholar 

  • Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti F, Caminiti R (2001) Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 11:513–527

    Article  PubMed  CAS  Google Scholar 

  • Merchant H, Georgopoulos AP (2006) Neurophysiology of perceptual and motor aspects of interception. J Neurophysiol 95:1–13

    Article  PubMed  Google Scholar 

  • Merchant H, Battaglia-Mayer A, Georgopoulos AP (2004a) Neural responses during interception of real and apparent circularly moving stimuli in motor cortex and area 7a. Cereb Cortex 14:314–331

    Article  PubMed  Google Scholar 

  • Merchant H, Battaglia-Mayer A, Georgopoulos AP (2004b) Neurophysiology of the parieto-frontal system during target interception. Neurol Clin Neurophysiol 2004:1

    PubMed  CAS  Google Scholar 

  • Messier J, Kalaska JF (1999) Comparison of variability of initial kinematics and endpoints of reaching movements. Exp Brain Res 125:139–152

    Article  PubMed  CAS  Google Scholar 

  • Messier J, Kalaska JF (2000) Covariation of primate dorsal premotor cell activity with direction and amplitude during a memorized-delay reaching task. J Neurophysiol 84:152–165

    PubMed  CAS  Google Scholar 

  • Mita A, Mushiake H, Shima K, Matsuzaka Y, Tanji J (2009) Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat Neurosci 12(4):502–507

    Google Scholar 

  • Moran DW, Schwartz AB (1999) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82:2676–2692

    PubMed  CAS  Google Scholar 

  • Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908

    PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Pisella L, Grea H, Tilikete C, Vighetto A, Desmurget M, Rode G, Boisson D, Rossetti Y (2000) An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 3:729–736

    Article  PubMed  CAS  Google Scholar 

  • Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci 4:317–323

    Article  PubMed  CAS  Google Scholar 

  • Rushworth MF, Taylor PC (2006) TMS in the parietal cortex: updating representations for attention and action. Neuropsychologia 44:2700–2716

    Article  PubMed  CAS  Google Scholar 

  • Rushworth MF, Ellison A, Walsh V (2001) Complementary localization and lateralization of orienting and motor attention. Nat Neurosci 4:656–661

    Article  PubMed  CAS  Google Scholar 

  • Rushworth MF, Johansen-Berg H, Gobel SM, Devlin JT (2003) The left parietal and premotor cortices: motor attention and selection. NeuroImage 20(Suppl 1):S89–S100

    Article  PubMed  Google Scholar 

  • Schwartz AB, Cui XT, Weber DJ, Moran DW (2006) Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52:205–220

    Article  PubMed  CAS  Google Scholar 

  • Strobach P, Abraham-Fuchs K, Härer W (1994) Event-synchronous cancellation of the heart interference in biomedical signals. IEEE Trans Biomed Eng 41:343–350

    Article  PubMed  CAS  Google Scholar 

  • Sun H, Frost BJ (1998) Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat Neurosci 1:296–303

    Article  PubMed  CAS  Google Scholar 

  • Taira M, Boline J, Smyrnis N, Georgopoulos AP, Ashe J (1996) On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force. Exp Brain Res 109:367–376

    Article  PubMed  CAS  Google Scholar 

  • Van Der Werf J, Jensen O, Fries P, Medendorp WP (2008) Gamma-band activity in human posterior parietal cortex encodes the motor goal during delayed prosaccades and antisaccades. J Neurosci 28:8397–8405

    Article  Google Scholar 

  • Waldert S, Preissl H, Demandt E, Braun C, Birbaumer N, Aertsen A, Mehring C (2008) Hand movement direction decoded from MEG and EEG. J Neurosci 28:1000–1008

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Frost BJ (1992) Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356:236–238

    Article  PubMed  CAS  Google Scholar 

  • Wenderoth N, Toni I, Bedeleem S, Debaere F, Swinnen SP (2006) Information processing in human parieto-frontal circuits during goal-directed bimanual movements. NeuroImage 31:264–278

    Article  PubMed  Google Scholar 

  • Williamson SJ, Kaufman L (1981) Biomagnetism. J Magn Magn Mater 22:129–201

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the following sources: The Carnegie Trust for the Universities of Scotland, UK, the ORSA, UK, the Tan Kah Khee Foundation, Singapore, the US Department of Veterans Affairs, and the American Legion Brain Sciences Chair.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Apostolos P. Georgopoulos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tan, HR.M., Leuthold, A.C., Lee, D.N. et al. Neural mechanisms of movement speed and tau as revealed by magnetoencephalography. Exp Brain Res 195, 541–552 (2009). https://doi.org/10.1007/s00221-009-1822-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-1822-5

Keywords

Navigation