Skip to main content
Log in

The speed of adaptation is dependent on the load type during target reaching by intact human subjects

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

Abstract

When lifting or moving a novel object, humans are routinely able to quickly characterize the nature of the unknown load and swiftly achieve the desired movement trajectory. It appears that both tactile and proprioceptive feedback systems help humans develop an accurate prediction of load properties and determine how associated limb segments behave during voluntary movements. While various types of limb movement information, such as position, velocity, acceleration, and manipulating forces, can be detected using human tactile and proprioceptive systems, we know little about how the central nervous system decodes these various types of movement data, and in which order or priority they are used when developing predictions of joint motion during novel object manipulation. In this study, we tested whether the ability to predict motion is different between position- (elastic), velocity- (viscous), and acceleration-dependent (inertial) loads imposed using a multiaxial haptic robot. Using this protocol, we can learn if the prediction of the motion model is optimized for one or more of these types of mechanical load. We examined ten neurologically intact subjects. Our key findings indicated that inertial and viscous loads showed the fastest adaptation speed, whereas elastic loads showed the slowest adaptation speed. Different speeds of adaptation were observed across different magnitudes of the load, suggesting that human capabilities for predicting joint motion and manipulating loads may vary systematically with different load types and load magnitudes. Our results imply that human capabilities for load manipulation seems to be most sensitive to and potentially optimized for inertial loads.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article. The datasets during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Analysis of all data in this study was performed using the Matlab software and the code, which will be available on reasonable request.

References

  • Bock O (1990) Load compensation in human goal-directed arm movements. Behav Brain Res 41:167–177

    Article  CAS  PubMed  Google Scholar 

  • Brindley G (1964) The use made by the cerebellum of the information that it receives from sense organs. Intern Brain Res Organ Bull 3:80

    Google Scholar 

  • Cherpin A, Kager S, Budhota A et al (2019) A preliminary study on the relationship between proprioceptive deficits and motor functions in chronic stroke patients. 2019 IEEE 16th International Conference on Rehabilitation Robotics (ICORR). IEEE, pp 465–470

    Chapter  Google Scholar 

  • Cooke J, Diggles VA (1984) Rapid error correction during human arm movements: evidence for central monitoring. J Mot Behav 16:348–363

    Article  CAS  PubMed  Google Scholar 

  • Cordo P, Carlton L, Bevan L, Carlton M, Kerr GK (1994) Proprioceptive coordination of movement sequences: role of velocity and position information. J Neurophysiol 71:1848–1861. https://doi.org/10.1152/jn.1994.71.5.1848

    Article  CAS  PubMed  Google Scholar 

  • Crevecoeur F, Thonnard J-L, Lefevre P (2020) A very fast time scale of human motor adaptation: within movement adjustments of internal representations during reaching. eNeuro. https://doi.org/10.1523/ENEURO.0149-19.2019

    Article  PubMed  PubMed Central  Google Scholar 

  • Feldman AG (2016) Active sensing without efference copy: referent control of perception. J Neurophysiol 116:960–976

    Article  PubMed  PubMed Central  Google Scholar 

  • Feldman AG, Levin MF (2009) The equilibrium-point hypothesis–past, present and future. Progress in motor control. Springer, pp 699–726

    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. https://doi.org/10.1007/s00221-008-1691-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flash T, Gurevich I (1997a) Arm trajectory generation and stiffness control during motor adaptation to external loads. Self-organization computational maps and motor control. Elsevier, pp 423–482

    Chapter  Google Scholar 

  • Flash T, Gurevich I (1997b) Models of motor adaptation and impedance control in human arm movements. Adv Psychol 119:423–481. https://doi.org/10.1016/S0166-4115(97)80015-5

    Article  Google Scholar 

  • Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5:1688–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forssberg H, Eliasson A, Kinoshita H, Johansson R, Westling G (1991) Development of human precision grip I: basic coordination of force. Exp Brain Res 85:451–457

    Article  CAS  PubMed  Google Scholar 

  • Forssberg H, Kinoshita H, Eliasson A, Johansson R, Westling G, Gordon A (1992) Development of human precision grip. Exp Brain Res 90:393–398

    Article  CAS  PubMed  Google Scholar 

  • Gribble PL, Scott SH (2002) Overlap of internal models in motor cortex for mechanical loads during reaching. Nature 417:938

    Article  CAS  PubMed  Google Scholar 

  • Gritsenko V, Krouchev NI, Kalaska JF (2007) Afferent input, efference copy, signal noise, and biases in perception of joint angle during active versus passive elbow movements. J Neurophysiol 98:1140–1154

    Article  CAS  PubMed  Google Scholar 

  • Häger-Ross C, Cole KJ, Johansson RS (1996) Grip-force responses to unanticipated object loading: load direction reveals body-and gravity-referenced intrinsic task variables. Exp Brain Res 110:142–150

    Article  PubMed  Google Scholar 

  • Huang FC, Patton JL (2011) Evaluation of negative viscosity as upper extremity training for stroke survivors. 2011 IEEE International Conference on Rehabilitation Robotics. IEEE, pp 1–6

    Google Scholar 

  • Hwang EJ, Shadmehr R (2005) Internal models of limb dynamics and the encoding of limb state. J Neural Eng 2:S266

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang EJ, Donchin O, Smith MA, Shadmehr R (2003) A gain-field encoding of limb position and velocity in the internal model of arm dynamics. PLoS Biol 1:e25

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang EJ, Smith MA, Shadmehr R (2006) Adaptation and generalization in acceleration-dependent force fields. Exp Brain Res 169:496–506

    Article  PubMed  Google Scholar 

  • Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564

    Article  CAS  PubMed  Google Scholar 

  • Johansson R, Westling G (1988) Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Exp Brain Res 71:59–71

    Article  CAS  PubMed  Google Scholar 

  • Johansson RS, Häger C, Riso R (1992) Somatosensory control of precision grip during unpredictable pulling loads. Exp Brain Res 89:192–203

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Linde RVD, Lammertse P, Frederiksen EB (2002) The HapticMaster, a new high-performance haptic interface. Proc. EuroHaptic, Edinburgh

    Google Scholar 

  • Lipták BG (2018) Instrument engineers handbook volume two: process control and optimization. CRC Press

    Book  Google Scholar 

  • Matthews P (1982) Where does Sherrington’s” muscular sense” originate? Muscles, joints, corollary discharges? Annu Rev Neurosci 5:189–218

    Article  CAS  PubMed  Google Scholar 

  • McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693

    Article  CAS  PubMed  Google Scholar 

  • Milner TE, Franklin DW (2005) Impedance control and internal model use during the initial stage of adaptation to novel dynamics in humans. J Physiol 567:651–664. https://doi.org/10.1113/jphysiol.2005.090449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowak DA, Hermsdörfer J, Topka H (2003) Deficits of predictive grip force control during object manipulation in acute stroke. J Neurol 250:850–860

    Article  PubMed  Google Scholar 

  • Pilon J-F, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67

    Article  PubMed  Google Scholar 

  • Sherrington C (1906) The integrative action of the nervous system. C. Scribner’s sons, New York

    Google Scholar 

  • Silva PS, Pereira P, Monteiro P, Silva PA, Vaz R (2013) Learning curve and complications of minimally invasive transforaminal lumbar interbody fusion. Neurosurg Focus 35:E7

    Article  PubMed  Google Scholar 

  • Sokolov AA, Miall RC, Ivry RB (2017) The cerebellum: adaptive prediction for movement and cognition. Trends in Cogn Sci 21:313–332. https://doi.org/10.1016/j.tics.2017.02.005

  • Stoeckmann TM, Sullivan KJ, Scheidt RA (2009) Elastic, viscous, and mass load effects on poststroke muscle recruitment and co-contraction during reaching: a pilot study. Phys Ther 89:665–678. https://doi.org/10.2522/ptj.20080128

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomi N, Gouko M, Ito K (2008) Impedance control complements imcomplete internal models under complex external dynamics. 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE, pp 5354–5357

    Chapter  Google Scholar 

  • Tseng Y-w, Diedrichsen Jr, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J neurophysiol 98:54–62

  • Uno Y, Kawato M, Suzuki R (1989) Formation and control of optimal trajectory in human multijoint arm movement. Biol Cybern 61:89–101. https://doi.org/10.1007/BF00204593

    Article  CAS  PubMed  Google Scholar 

  • Van Der Linde RQ, Lammertse P (2003) HapticMaster-a generic force controlled robot for human interaction. Ind Robot 30:515–524. https://doi.org/10.1108/01439910310506783

    Article  Google Scholar 

  • Vato A, Szymanski FD, Semprini M, Mussa-Ivaldi FA, Panzeri S (2014) A bidirectional brain-machine interface algorithm that approximates arbitrary force-fields. PLoS ONE. https://doi.org/10.1371/journal.pone.0091677

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidoni ED, Boyd LA (2009) Preserved motor learning after stroke is related to the degree of proprioceptive deficit. Behav Brain Funct 5:1–10

    Article  Google Scholar 

  • Westling G, Johansson R (1984) Factors influencing the force control during precision grip. Exp Brain Res 53:277–284

    Article  CAS  PubMed  Google Scholar 

  • Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347. https://doi.org/10.1016/S1364-6613(98)01221-2

    Article  CAS  PubMed  Google Scholar 

  • Zhang L-Q, Son J, Park H-S, Kang SH, Lee Y, Ren Y (2017) Changes of shoulder, elbow, and wrist stiffness matrix post stroke. IEEE Trans Neural Syst Rehabil Eng 25:844–851

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This project was supported under grant 90RES5013 from the U.S. Department of Health and Human Services, Administration on Community Living, National Institute on Disability, Independent Living and Rehabilitation Research. This work was also supported by the Korea Institute of Science and Technology (KIST) Institutional Program (Project no. 2E31110).

Funding

This project was supported under grant 90RES5013 from the U.S. Department of Health and Human Services, Administration on Community Living, National Institute on Disability, Independent Living and Rehabilitation Research. This work was also supported by the Korea Institute of Science and Technology (KIST) Institutional Program (Project no. 2E31110).

Author information

Authors and Affiliations

Authors

Contributions

All authors were heavily involved in study design, developing experimental apparatus, conducting an experiment, analyzing data, and writing the manuscript. KO carried out the experiments, performed statistical analysis, and drafted the manuscript. WZR designed the study and helped to write the manuscript. JC developed the experimental apparatus, helped to analyze the data, and finalized the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Junho Choi.

Ethics declarations

Conflict of interest

There are no conflicts of interest to declare.

Ethical approval

All subjects signed an informed consent form which was approved by the Northwestern University Institutional Review Board (IRB) before the experiments. This information was also described in the methods section.

Consent for participate

All subjects signed an informed consent form, which was approved by the Northwestern University Institutional Review Board (IRB) before the experiments.

Consent for publication

All images, including subjects, were de-identified and added to this manuscript with subjects’ consent.

Additional information

Communicated by Bill J Yates.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oh, K., Rymer, W.Z. & Choi, J. The speed of adaptation is dependent on the load type during target reaching by intact human subjects. Exp Brain Res 239, 3091–3104 (2021). https://doi.org/10.1007/s00221-021-06189-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-021-06189-3

Keywords

Navigation