Skip to main content

Advertisement

Log in

Two-phase strategy of neural control for planar reaching movements: I. XY coordination variability and its relation to end-point variability

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

Abstract

A quantitative model of optimal transport–aperture coordination (TAC) during reach-to-grasp movements has been developed in our previous studies. The utilization of that model for data analysis allowed, for the first time, to examine the phase dependence of the precision demand specified by the CNS for neurocomputational information processing during an ongoing movement. It was shown that the CNS utilizes a two-phase strategy for movement control. That strategy consists of reducing the precision demand for neural computations during the initial phase, which decreases the cost of information processing at the expense of lower extent of control optimality. To successfully grasp the target object, the CNS increases precision demand during the final phase, resulting in higher extent of control optimality. In the present study, we generalized the model of optimal TAC to a model of optimal coordination between X and Y components of point-to-point planar movements (XYC). We investigated whether the CNS uses the two-phase control strategy for controlling those movements, and how the strategy parameters depend on the prescribed movement speed, movement amplitude and the size of the target area. The results indeed revealed a substantial similarity between the CNS’s regulation of TAC and XYC. First, the variability of XYC within individual trials was minimal, meaning that execution noise during the movement was insignificant. Second, the inter-trial variability of XYC was considerable during the majority of the movement time, meaning that the precision demand for information processing was lowered, which is characteristic for the initial phase. That variability significantly decreased, indicating higher extent of control optimality, during the shorter final movement phase. The final phase was the longest (shortest) under the most (least) challenging combination of speed and accuracy requirements, fully consistent with the concept of the two-phase control strategy. This paper further discussed the relationship between motor variability and XYC variability.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Notes

  1. Initial movement direction is often measured at a certain time after the movement onset, such as 100 ms (Bernier et al. 2005; Hinder et al. 2010) and 200 ms (Heuer and Hegele 2008), or at a certain kinematic landmark, such as peak velocity (Hinder et al. 2010; Wang and Sainburg 2005). The average distance of hand position at 180 ms into movements from the movement onset was 3.3 mm for the small-target, short-distance, slow-speed condition and 56.0 mm for the large-target, short-distance, maximum-speed condition. This wide range of the distance from the movement onset across different conditions prevented us from using a certain time from the movement onset or peak velocity for this measurement. It is because the initial direction measurement is unstable at a very short distance from the starting position (i.e., 3.3 mm) and because the angle of initial movement direction significantly varies depending on the distance from the starting position that is used for the measurement. Therefore, we employed a fix distance (3 cm), which was close to the average distance across the conditions at 180 ms into the movement.

  2. To someone who is used to thinking about motor control in terms of kinematic parameters as continuous sequences of values within a specific time interval, it might seem that, since, for instance, acceleration as a function of time can be computed as a time derivative of velocity, it must be sufficient to include only one such parameter in equations. In the case of the equation describing XY coordination, however, instantaneous values of such parameters are involved, and therefore, a different logic applies. Knowledge of hand velocity at a certain time point t in general does not allow one to calculate hand acceleration and vice versa. For this reason, these kinematic variables are viewed in theoretical mechanics as state coordinates independent of each other.

  3. It is important to acknowledge that the correlation matrix should not be, in general, used for this purpose. This is so because the variance of one or more movement parameters in general can be very small. For example, in the case of XY reaching movement, the stylus tip trajectory can be arranged along the x axis with negligible variation along the Y axis. In this example, the XYC model k y y − y 0 = 0, where k y  = 1 and y 0 is the average Y coordinate, accurately describes the movement, since the variation of y around y 0 is very small. On the first sight, it may seem incorrect to state that an optimal XYC is observed in this example. However, simply by rotating the XY coordinate system 45 degrees (clockwise or counterclockwise), one can obtain a trajectory where any displacement along the x axis is almost exactly equal (in its absolute value) to the corresponding displacement along the Y axis, thus showing a near-perfect XYC. The method of determining the XYC model’s precision obviously should not depend on the choice of the XY coordinate system.

  4. To see that, note that the total variance is equal to the sum of the diagonal elements (i.e., trace) of the covariance matrix, and the sum of the eigenvalues is equal to the above sum.

  5. This component does not reflect any significant nonoptimality of movement control if it is determined by the variability of the end-point within the boundaries of the target area. This is so because as long as the end-point is within the target area, its deviation from the area’s center does not increase the cost of a target acquisition error.

References

  • Bays PM, Wolpert DM (2007) Computational principles of sensorimotor control that minimize uncertainty and variability. J Physiol 578:387–396

    Article  PubMed  CAS  Google Scholar 

  • Bédard P, Proteau L (2004) On-line vs. off-line utilization of peripheral visual afferent information to ensure spatial accuracy of goal-directed movements. Exp Brain Res 158:75–85

    Article  PubMed  Google Scholar 

  • Bernier PM, Chua R, Franks IM (2005) Is proprioception calibrated during visually guided movements? Exp Brain Res 167:292–296

    Article  PubMed  Google Scholar 

  • Bertram CP, Lemay M, Stelmach GE (2005) The effect of Parkinson’s disease on the control of multi-segmental coordination. Brain Cogn 57:16–20

    Article  PubMed  Google Scholar 

  • Darling WG, Stephenson M (1993) Directional effects on variability of upper limb movements. In: Newell KM, Corcos DM (eds) Variability and motor control. Human Kinetics, Champaign, pp 65–88

    Google Scholar 

  • Davis JH (2002) Foundations of deterministic and stochastic control. Birkhäuser, Boston

    Book  Google Scholar 

  • Elliott D, Helsen WF, Chua R (2001) A century later: Woodworth’s (1899) two-component model of goal-directed aiming. Psychol Bull 127:342–357

    Article  PubMed  CAS  Google Scholar 

  • Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9:292–303

    Article  PubMed  CAS  Google Scholar 

  • Fradet L, Lee G, Dounskaia N (2008) Origins of submovements during pointing movements. Acta Psychol (Amst) 129:91–100

    Article  Google Scholar 

  • Haggard P, Wing AM (1997) On the hand transport component of prehensile movements. J Mot Behav 29:282–287

    Article  PubMed  CAS  Google Scholar 

  • Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784

    Article  PubMed  CAS  Google Scholar 

  • Heuer H, Hegele M (2008) Adaptation to visuomotor rotations in younger and older adults. Psychol Aging 23:190–202

    Article  PubMed  Google Scholar 

  • Hinder MR, Riek S, Tresilian JR, de Rugy A, Carson RG (2010) Real-time error detection but not error correction drives automatic visuomotor adaptation. Exp Brain Res 201:191–207

    Article  PubMed  Google Scholar 

  • Ho T, Brown S, van Maanen L, Forstmann BU, Wagenmakers EJ, Serences JT (2012) The optimality of sensory processing during the speed-accuracy tradeoff. J Neurosci 32:7992–8003

    Article  PubMed  CAS  Google Scholar 

  • Hoff B, Arbib MA (1993) Models of trajectory formation and temporal interaction of reach and grasp. J Mot Behav 25:175–192

    Article  PubMed  Google Scholar 

  • Jolliffe IT (2002) Principal component analysis. Series: Springer series in statistics. Springer, New York

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727

    Article  PubMed  CAS  Google Scholar 

  • Khan MA, Franks IM (2003) Online versus offline processing of visual feedback in the production of component submovements. J Mot Behav 35:285–295

    Article  PubMed  Google Scholar 

  • Khan MA, Franks IM, Goodman D (1998) The effect of practice on the control of rapid aiming movements: evidence for an interdependency between programming and feedback processing. Q J Exp Psychol A 51:425–443

    Google Scholar 

  • Khan MA, Lawrence G, Fourkas A, Franks IM, Elliott D, Pembroke S (2003) Online versus offline processing of visual feedback in the control of movement amplitude. Acta Psychol (Amst) 113:83–97

    Article  Google Scholar 

  • Khan MA, Franks IM, Elliott D, Lawrence GP, Chua R, Bernier PM, Hansen S, Weeks DJ (2006) Inferring online and offline processing of visual feedback in target-directed movements from kinematic data. Neurosci Biobehav Rev 30:1106–1121

    Article  PubMed  Google Scholar 

  • Meyer DE, Abrams RA, Kornblum S, Wright CE, Smith JEK (1988) Optimality in human motor performance: ideal control of rapid aimed movements. Psychol Rev 95:340–370

    Article  PubMed  CAS  Google Scholar 

  • Naslin P (1969) Essentials of optimal control. Boston Technical Publishers, Cambridge

    Google Scholar 

  • Newell KM, Corcos DM (1993) Issues in variability and motor control. In: Newell KM, Corcos DM (eds) Variability and motor control. Human Kinetics, Champaign, pp 1–12

    Google Scholar 

  • Papoulis A (1990) Probability and statistics. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Rand MK, Smiley-Oyen AL, Shimansky YP, Bloedel JR, Stelmach GE (2006) Control of aperture closure during reach-to-grasp movements in Parkinson’s disease. Exp Brain Res 168:131–142

    Article  PubMed  CAS  Google Scholar 

  • Rand MK, Shimansky YP, Hossain ABM, Stelmach GE (2008) Quantitative model of transport-aperture coordination during reach-to-grasp movements. Exp Brain Res 188:263–274

    Article  PubMed  Google Scholar 

  • Rand MK, Lemay M, Squire LM, Shimansky YP, Stelmach GE (2010a) Control of aperture closure initiation during reach-to-grasp movements under manipulations of visual feedback and trunk involvement in Parkinson’s disease. Exp Brain Res 201:509–525

    Article  PubMed  Google Scholar 

  • Rand MK, Shimansky YP, Hossain ABMI, Stelmach GE (2010b) Phase dependence of transport-aperture coordination variability reveals control strategy of reach-to-grasp movements. Exp Brain Res 207:49–63

    Article  PubMed  Google Scholar 

  • Rand MK, Van Gemmert AWA, Hossain ABMI, Shimansky YP, Stelmach GE (2012) Control of aperture closure initiation during trunk-assisted reach-to-grasp movements. Exp Brain Res 219:293–304

    Article  PubMed  Google Scholar 

  • Shimansky YP (2000) Spinal motor control system incorporates an internal model of limb dynamics. Biol Cybern 83:379–389

    Article  PubMed  CAS  Google Scholar 

  • Shimansky YS, Rand MK (2012) Two-phase strategy of controlling motor coordination determined by task performance optimality. Biol Cybern (in press)

  • Shimansky YP, Kang T, He J (2004) A novel model of motor learning capable of developing an optimal movement control law online from scratch. Biol Cybern 90:133–145

    Google Scholar 

  • Teasdale N, Bard C, Fleury M, Young D, Proteau L (1993) Determining movement onsets from temporal series. J Mot Behav 25:97–106

    Article  PubMed  CAS  Google Scholar 

  • Tinjust D, Proteau L (2009) Modulation of the primary impulse of spatially-constrained video-aiming movements. Hum Mov Sci 28:155–168

    Article  PubMed  Google Scholar 

  • Todorov E, Jordan MI (2002) Signal-dependent noise determines motor planning. Nat Neurosci 5:1226–1235

    Article  PubMed  CAS  Google Scholar 

  • Valero-Cuevas FJ, Venkadesan M, Todorov E (2009) Structured variability of muscle activations supports the minimal intervention principle of motor control. J Neurophysiol 102:59–68

    Article  PubMed  Google Scholar 

  • van Beers RJ, Haggard P, Wolpert DM (2004) The role of execution noise in movement variability. J Neurophysiol 91:1050–1063

    Article  PubMed  Google Scholar 

  • Vindras P, Viviani P (1998) Frames of reference and control parameters in visuomanual pointing. J Exp Psychol Hum Percept Perform 24:569–591

    Article  PubMed  CAS  Google Scholar 

  • Viviani P, Flash T (1995) Minimum-jerk, two-thirds power law, and isochrony: converging approaches to movement planning. J Exp Psychol Hum Percept Perform 21:32–53

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Sainburg RL (2005) Adaptation to visuomotor rotations remaps movement vectors, not final positions. J Neurosci 25:4024–4030

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3:1212–1217

    Google Scholar 

  • Woodworth RS (1899) The accuracy of voluntary movement. Psychol Rev 3(Suppl 2):1–114

    Google Scholar 

  • Yang F, Feldman AG (2010) Reach-to-grasp movement as a minimization process. Exp Brain Res 201:75–92

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Herbert Heuer for his helpful comments on an earlier version of the manuscript. We also thank Eva Hanisch, Maia Iobidze, Jennifer Stube and Sarah Jacob for their help in data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miya K. Rand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rand, M.K., Shimansky, Y.P. Two-phase strategy of neural control for planar reaching movements: I. XY coordination variability and its relation to end-point variability. Exp Brain Res 225, 55–73 (2013). https://doi.org/10.1007/s00221-012-3348-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-012-3348-5

Keywords

Navigation