Abstract
Sensorimotor integration is essential for controlling movement and acquiring new motor tasks in humans. The aim of this project was to understand how lower limb proprioceptive sense contributes to the acquisition of a skilled walking task. We assessed lower limb joint position and movement detection sense in healthy human subjects using the Lokomat robotic exoskeleton. Subjects walked on a treadmill to practice a skilled motor task (200 trials) requiring them to match their foot height during the swing phase to the height of a virtual obstacle displayed on a monitor in front of them. Subjects were given visual feedback on their error relative to the obstacle height after it was crossed. Lower limb joint position sense was related to the final performance error, but not the learning rate of the skilled walking task. The findings from this study support the role of lower limb proprioceptive sense on locomotor skill performance in healthy adult subjects.
Similar content being viewed by others
References
Andujar J, Lajoie K, Drew T (2010; 2009) A contribution of area 5 of the posterior parietal cortex to the planning of visually guided locomotion: limb-specific and limb-independent effects. J Neurophysiol 103:986–1006. doi:10.1152/jn.00912.2009
Boerboom AL, Huizinga MR, Kaan WA, Stewart RE, Hof AL, Bulstra SK, Diercks RL (2008) Validation of a method to measure the proprioception of the knee. Gait Posture 28:610–614. doi:10.1016/j.gaitpost.2008.04.007
Burge J, Ernst MO, Banks MS (2008) The statistical determinants of adaptation rate in human reaching. J Vis 8(20):1
Burke D, Gandevia SC, Macefield G (1988) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol (Lond) 402:347–361. doi:10.1113/jphysiol.1988.sp017208
Castro LNG, Hadjiosif AM, Hemphill MA, Smith MA (2014) Environmental consistency determines the rate of motor adaptation. Curr Biol 24:1050–1061. doi:10.1016/j.cub.2014.03.049
Chisholm AE, Domingo A, Jeyasurya J, Lam T (2015) Quantification of lower extremity kinesthesia deficits using a robotic exoskeleton in people with a spinal cord injury. Neurorehabil Neural Repair. doi:10.1177/1545968315591703
Corrigan J, Cashman W, Brady M (1992) Proprioception in the cruciate deficient knee. J Bone Joint Surg Br 74:247–250
Darainy M, Vahdat S, Ostry DJ (2013) Perceptual learning in sensorimotor adaptation. J Neurophysiol 110(9):2152–2162. doi:10.1152/jn.00439.2013
Della-Maggiore V, Malfait N, Ostry DJ, Paus T (2004) Stimulation of the posterior parietal cortex interferes with arm trajectory adjustments during the learning of new dynamics. J Neurosci 24:9971–9976. doi:10.1523/JNEUROSCI.2833-04.2004
Domingo A, Lam T (2014) Reliability and validity of using the Lokomat to assess lower limb joint position sense in people with incomplete spinal cord injury. J Neuroeng Rehabil 11:167. doi:10.1186/1743-0003-11-167
Elias LJ, Bryden MP, Bulman-Fleming MB (1998) Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia 36:37–43. doi:10.1016/S0028-3932(97)00107-3
Erni T, Dietz V (2001) Obstacle avoidance during human walking: learning rate and cross-modal transfer. J Physiol (Lond) 534:303–312. doi:10.1111/j.1469-7793.2001.00303.x
Friden T et al (2001) Review of knee proprioception and the relation to extremity function after an anterior cruciate ligament rupture. J Orthop Sports Phys Therapy 31:567–576
Fridén T et al (1996) Proprioception in the nearly extended knee. Measurements of position and movement in healthy individuals and in symptomatic anterior cruciate ligament injured patients. Knee Surg Sports Traumatol Arthrosc 4:217–224. doi:10.1007/BF01567966
Ghez C, Gordon J, Ghilardi MF (1995) Impairments of reaching movements in patients without proprioception. II. effects of visual information on accuracy. J Neurophysiol 73(1):361
Grasso R, Bianchi L, Lacquaniti F (1998) Motor patterns for human gait: backward versus forward locomotion. J Neurophysiol 80:1868–1885
Grasso R, Zago M, Lacquaniti F (2000) Interactions between posture and locomotion: motor patterns in humans walking with bent posture versus erect posture. J Neurophysiol 83:288–300
Graziano MSA (1999) Where is my arm? the relative role of vision and proprioception in the neuronal representation of limb position. Proc Natl Acad Sci U S A 96(18):10418–10421. doi:10.1073/pnas.96.18.10418
Han J, Waddington G, Anson J, Adams R (2015) Level of competitive success achieved by elite athletes and multi-joint proprioceptive ability. J Sci Med Sport 18:77–81. doi:10.1016/j.jsams.2013.11.013
Hasan Z (1992) Role of proprioceptors in neural control. Curr Opin Neurobiol 2:824–829. doi:10.1016/0959-4388(92)90140-G
Ivanenko YP, Grasso R, Macellari V, Lacquaniti F (2002) Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. J Neurophysiol 87:3070–3089. doi:10.1152/jn.00815.2001
Lacquaniti F, Ivanenko Y, Zago M (2002) Kinematic control of walking. Arch Ital Biol 140:263–272
Lajoie K, Bloomfield L, Nelson F, Suh J, Marigold D (2012) The contribution of vision, proprioception, and efference copy in storing a neural representation for guiding trail leg trajectory over an obstacle. J Neurophysiol 107:2283–2293. doi:10.1152/jn.00756.2011
Lam T, Dietz V (2004) Transfer of motor performance in an obstacle avoidance task to different walking conditions. J Neurophysiol 92:2010–2016. doi:10.1152/jn.00397.2004
Marigold DS (2008) Role of peripheral visual cues in online visual guidance of locomotion. Exerc Sport Sci Rev 36:145–151. doi:10.1097/JES.0b013e31817bff72
Marigold DS, Andujar JE, Lajoie K, Drew T (2011) Chapter 6—Motor planning of locomotor adaptations on the basis of vision the role of the posterior parietal cortex. Prog Brain Res 188:83–100
Ostry DJ, Darainy M, Mattar AAG, Wong J, Gribble PL (2010) Somatosensory plasticity and motor learning. J Neurosci 30:5384–5393. doi:10.1523/JNEUROSCI.4571-09.2010
Pavlides C, Miyashita E, Asanuma H (1993) Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J Neurophysiol 70:733–741
Ribeiro F, Oliveira J (2011). Factors influencing proprioception: What do they reveal? In: Vaclav K (ed) Biomechanics in applications. ISBN: 978-953-307-969-1, InTech. doi: 10.5772/20335. http://www.intechopen.com/books/biomechanics-in-applications/factors-influencing-proprioception-what-do-they-reveal
Sakamoto T, Arissian K, Asanuma H (1989) Functional role of the sensory cortex in learning motor skills in cats. Brain Res 503:258–264. doi:10.1016/0006-8993(89)91672-7
Schmidt RA, Lee TD (2011) Motor control and learning: a behavioral emphasis, 5th ed. Human Kinetics, Champaign, IL
Selfe J, Callaghan M, McHenry A, Richards J, Oldham J (2006) An investigation into the effect of number of trials during proprioceptive testing in patients with patellofemoral pain syndrome. J Orthop Res 24:1218–1224. doi:10.1002/jor.20127
Sherrington CS (1907) On the proprioceptive system, especially in its reflex aspect. Brain 29:467–482. doi:10.1093/brain/29.4.467
Smith TO, Davies L, Hing CB (2013) A systematic review to determine the reliability of knee joint position sense assessment measures. Knee 20:162. doi:10.1016/j.knee.2012.06.010
Sober SJ, Sabes PN (2008) Flexible strategies for sensory integration during motor planning. Nat Neurosci 8:490–497. doi:10.1038/nn1427
van Hedel HJA, Biedermann M, Erni T, Dietz V (2002) Obstacle avoidance during human walking: transfer of motor skill from one leg to the other. J Physiol (Lond) 543:709–717. doi:10.1113/jphysiol.2002.018473
Vidoni ED, Boyd LA (2009) Preserved motor learning after stroke is related to the degree of proprioceptive deficit. Behav Brain Funct (BBF) 5:36. doi:10.1186/1744-9081-5-36
Wei K, Körding K (2010) Uncertainty of feedback and state estimation determines the speed of motor adaptation. Front Comput Neurosci 4:11. doi:10.3389/fncom.2010.00011
Winter D (1992) Foot trajectory in human gait: a precise and multifactorial motor control task. Phys Ther 72:45–53
Wong JD, Wilson ET, Gribble PL (2011) Spatially selective enhancement of proprioceptive acuity following motor learning. J Neurophysiol 105:2512–2521. doi:10.1152/jn.00949.2010
Wu HG, Miyamoto YR, Castro LNG, Ölveczky BP, Smith MA (2014) Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat Neurosci 17:312. doi:10.1038/nn.3616
Acknowledgments
The authors thank Franco Chan for his valuable technical assistance during this study. Funding for this study was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant 355928) and an NSERC Undergraduate Student Research Award to TQ.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Rights and permissions
About this article
Cite this article
Qaiser, T., Chisholm, A.E. & Lam, T. The relationship between lower limb proprioceptive sense and locomotor skill acquisition. Exp Brain Res 234, 3185–3192 (2016). https://doi.org/10.1007/s00221-016-4716-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4716-3