Spinal Mechanisms May Provide a Combination of Intermittent and Continuous Control of Human Posture: Predictions from a Biologically Based Neuromusculoskeletal Model

PLoS Computational Biology

Volumn 10, Issue 11, 2014, Pages

  Elias, Leonardo Abdala ^a   Watanabe, Renato Naville ^a   Kohn, André Fabio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; FEEDBACK; INVERTED PENDULUM; NEURONS; STOCHASTIC SYSTEMS;

CONTINUOUS CONTROL; HUMAN MODELLING; HUMAN POSTURES; INTERMITTENT CONTROLS; INVERTED PENDULUM; MOTOR NEURONS; NEUROMUSCULOSKELETAL MODELS; POSTURAL CONTROL; POSTURE PREDICTION; THEORETICAL MODELING;

MUSCLE;

ARTICLE; BIOMECHANICS; BODY POSTURE; CONTROLLED STUDY; ELECTROMYOGRAM; GASTROCNEMIUS MUSCLE; HUMAN; INTERNEURON; LEG MUSCLE; MATHEMATICAL MODEL; MOTONEURON; MOTOR CONTROL; MUSCLE CELL; NEUROMUSCULOSKELETAL MODEL; PROPRIOCEPTION; SENSORY NERVE; SIMULATION; SOLEUS MUSCLE; SPINAL CORD NERVE CELL; STANDING; STOCHASTIC MODEL; ADULT; BIOLOGICAL MODEL; BIOLOGY; FEEDBACK SYSTEM; MUSCULOSKELETAL FUNCTION; PHYSIOLOGY; REPRODUCIBILITY; SPINAL CORD; TORQUE; YOUNG ADULT;

ADULT; COMPUTATIONAL BIOLOGY; FEEDBACK, PHYSIOLOGICAL; HUMANS; MODELS, BIOLOGICAL; MOTOR NEURONS; MUSCULOSKELETAL PHYSIOLOGICAL PHENOMENA; POSTURE; REPRODUCIBILITY OF RESULTS; SPINAL CORD; TORQUE; YOUNG ADULT;

EID: 84912144707     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003944     Document Type: Article

References (92)

1. Macpherson JM, Horak FB (2013) Posture. In: Kandel ER, Schwartz JH, Jessell TM, Siegelbaum SA, Hudspeth AJ, editors, Principles of neural science, New York: McGraw-Hill, chapter 41. 5 edition, pp. 935–959.
2. Simoneau GG, Ulbrecht JS, Derr JA, Cavanagh PR, (1995) Role of somatosensory input in the control of human posture. Gait & Posture 3: 115–122.
3. Baloh RW, Jacobson KM, Beykirch K, Honrubia V, (1998) Static and dynamic posturography in patients with vestibular and cerebellar lesions. Archives of Neurology 55: 649–654.
4. Peterka RJ, (2000) Postural control model interpretation of stabilogram diffusion analysis. Biological Cybernetics 82: 335–343.
5. Maurer C, Peterka RJ, (2005) A new interpretation of spontaneous sway measures based on a simple model of human postural control. Journal of Neurophysiology 93: 189–200.
6. van der Kooij H, de Vlugt E, (2007) Postural responses evoked by platform pertubations are dominated by continuous feedback. Journal of Neurophysiology 98: 730–743.
7. Fitzpatrick R, Burke D, Gandevia SC, (1996) Loop gain of reflexes controlling human standing measured with the use of postural and vestibular disturbances. Journal of Neurophysiology 76: 3994–4008.
8. Morasso PG, Schieppati M, (1999) Can muscle stiffness alone stabilize upright standing? Journal of Neurophysiology 82: 1622–1626.
9. Gatev P, Thomas S, Kepple T, Hallett M, (1999) Feedforward ankle strategy of balance during quiet stance in adults. The Journal of Physiology 514: 915–928.
10. Bottaro A, Casadio M, Morasso PG, Sanguineti V, (2005) Body sway during quiet standing: is it the residual chattering of an intermittent stabilization process? Human Movement Science 24: 588–615.
11. Bottaro A, Yasutake Y, Nomura T, Casadio M, Morasso P, (2008) Bounded stability of the quiet standing posture: an intermittent control model. Human Movement Science 27: 473–95.
12. Gawthrop P, Loram I, Lakie M, Gollee H, (2011) Intermittent control: a computational theory of human control. Biological Cybernetics 104: 31–51.
13. Loram ID, Gollee H, Lakie M, Gawthrop PJ, (2011) Human control of an inverted pendulum: is continuous control necessary? Is intermittent control effective? Is intermittent control physiological? Journal of Physiology 589: 307–324.
14. Vieira TM, Loram ID, Muceli S, Merletti R, Farina D, (2012) Recruitment of motor units in the medial gastrocnemius muscle during human quiet standing: is recruitment intermittent? What triggers recruitment? Journal of Neurophysiology 107: 666–676.
15. van de Kamp C, Gawthrop PJ, Gollee H, Loram ID, (2013) Refractoriness in sustained visuo-manual control: is the refractory duration intrinsic or does it depend on external system properties? PLoS Computational Biology 9: e1002843.
16. Héroux ME, Dakin CJ, Luu BL, Inglis JT, Blouin JS, (2014) Absence of lateral gastrocnemius activity and differential motor unit behavior in soleus and medial gastrocnemius during standing balance. Journal of Applied Physiology 116: 140–8.
17. Cabrera J, Milton J, (2002) On-Off intermittency in a human balancing task. Physical Review Letters 89: 158702.
18. Alexandrov AV, Frolov AA, Horak FB, Carlson-Kuhta P, Park S, (2005) Feedback equilibrium control during human standing. Biological Cybernetics 93: 309–322.
19. Kohn AF, (2005) Cross-correlation between EMG and center of gravity during quiet stance: theory and simulations. Biological Cybernetics 93: 382–388.
20. Masani K, Vette AH, Popovic MR, (2006) Controlling balance during quiet standing: proportional and derivative controller generates preceding motor command to body sway position observed in experiments. Gait & Posture 23: 164–172.
21. Kuo AD, (2005) An optimal state estimation model of sensory integration in human postural balance. Journal of Neural Engineering 2: S235–49.
22. van der Kooij H, Jacobs R, Koopman B, Grootenboer H, (1999) A multisensory integration model of human stance control. Biological Cybernetics 80: 299–308.
23. van der Kooij H, Jacobs R, Koopman B, Van der Helm F, (2001) An adaptive model of sensory integration in a dynamic environment applied to human stance control. Biological Cybernetics 84: 103–115.
24. Suzuki Y, Nomura T, Casadio M, Morasso P, (2012) Intermittent control with ankle, hip, and mixed strategies during quiet standing: a theoretical proposal based on a double inverted pendulum model. Journal of Theoretical Biology 310: 55–79.
25. Nomura T, Oshikawa S, Suzuki Y, Kiyono K, Morasso P, (2013) Modeling human postural sway using an intermittent control and hemodynamic perturbations. Mathematical Biosciences 245: 86–95.
26. Gage WH, Winter DA, Frank JS, Adkin AL, (2004) Kinematic and kinetic validity of the inverted pendulum model in quiet standing. Gait & Posture 19: 124–132.
27. Scott SH, Loeb GE, (1994) The computation of position sense from spindles in monoarticular and multiarticular muscles. Journal of Neuroscience 14: 7529–7540.
28. Proske U, Wise AK, Gregory JE, (2000) The role of muscle receptors in the detection of movements. Progress in Neurobiology 60: 85–96.
29. Di Giulio I, Maganaris CN, Baltzopoulos V, Loram ID, (2009) The proprioceptive and agonist roles of gastrocnemius, soleus and tibialis anterior muscles in maintaining human upright posture. The Journal of Physiology 587: 2399–2416.
30. Day JT, Lichtwark GA, Cresswell AG, (2013) Tibialis anterior muscle fascicle dynamics adequately represent postural sway during standing balance. Journal of Applied Physiology 115: 1742–50.
31. Loram ID, Maganaris CN, Lakie M, (2005) Active, non-spring-like muscle movements in human postural sway: how might paradoxical changes in muscle length be produced? Journal of Physiology 564: 281–293.
32. Schuurmans J, van der Helm FC, Schouten AC, (2010) Relating reflex gain modulation in posture control to underlying neural network properties using a neuromusculoskeletal model. Journal of Computational Neuroscience 30: 555–65.
33. Stienen AHA, Schouten AC, Schuurmans J, van der Helm FCT, (2007) Analysis of reflex modulation with a biologically realistic neural network. Journal of Computational Neuroscience 23: 333–348.
34. Elias LA, Watanabe RN, Kohn AF (2013) Large-scale neuromusculoskeletal model used to investigate neurophysiological mechanisms behind upright stance control. In: 43rd Annual Meeting of the Society for Neuroscience. San Diego, p. 293.07.
35. Elias LA, Watanabe RN, Kohn AF (2014) The role of reciprocal inhibition on human postural control. In: Proceedings of the Bernstein Conference 2014. Göttingen: BFNT/BCCN, pp. 185–186. doi:10.12751/nncn.bc2014.0202.
36. Mezzarane RA, Kohn AF, (2007) Control of upright stance over inclined surfaces. Experimental Brain Research 180: 377–388.
37. Taube W, Gruber M, Beck S, Faist M, Gollhofer A, et al. (2007) Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiologica 189: 347–358.
38. Ushiyama J, Takahashi Y, Ushiba J, (2010) Muscle dependency of corticomuscular coherence in upper and lower limb muscles and training-related alterations in ballet dancers and weightlifters Muscle dependency of corticomuscular coherence in upper and lower limb muscles and training-related alterat. Journal of Applied Physiology 109: 1086–95.
39. Lawrence EL, Fassola I, Werner I, Leclercq C, Valero-Cuevas FJ, (2014) Quantification of dexterity as the dynamical regulation of instabilities: comparisons across gender, age, and disease. Frontiers in Neurology 5: 53.
40. Murnaghan CD, Squair JW, Chua R, Inglis JT, Carpenter MG, (2014) Cortical contributions to control of posture during unrestricted and restricted stance. Journal of Neurophysiology 111: 1920–6.
41. Cisi RRL, Kohn AF, (2008) Simulation system of spinal cord motor nuclei and associated nerves and muscles, in a Web-based architecture. Journal of Computational Neuroscience 25: 520–542.
42. Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM, (1996) Measures of postural steadiness: Differences between healthy young and elderly adults. IEEE Transactions on Biomedical Engineering 43: 956–966.
43. Masani K, Popovic MR, Nakazawa K, Kouzaki M, Nozaki D, (2003) Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. Journal of Neurophysiology 90: 3774–82.
44. Prochazka A, Hulliger M, Zangger P, Appenteng K, (1985) ‘Fusimotor set’: new evidence for alpha-independent control of gamma-motoneurones during movement in the awake cat. Brain Research 339: 136–40.
45. Windhorst U, (2007) Muscle proprioceptive feedback and spinal networks. Brain Research Bulletin 73: 155–202.
46. Casadio M, Morasso PG, Sanguineti V, (2005) Direct measurement of ankle stiffness during quiet standing: implications for control modelling and clinical application. Gait & Posture 21: 410–424.
47. Loram ID, Maganaris CN, Lakie M, (2007) The passive, human calf muscles in relation to standing: the non-linear decrease from short range to long range stiffness. Journal of Physiology-London 584: 661–675.
48. Loram ID, Maganaris CN, Lakie M, (2007) The passive, human calf muscles in relation to standing: the short range stiffness lies in the contractile component. Journal of Physiology-London 584: 677–692.
49. van Soest AJ, Rozendaal LA, (2008) The inverted pendulum model of bipedal standing cannot be stabilized through direct feedback of force and contractile element length and velocity at realistic series elastic element stiffness. Biological Cybernetics 99: 29–41.
50. van de Kamp C, Gawthrop PJ, Gollee H, Lakie M, Loram ID, (2013) Interfacing sensory input with motor output: does the control architecture converge to a serial process along a single channel? Frontiers in Computational Neuroscience 7: 55.
51. Loram ID, van de Kamp C, Lakie M, Gollee H, Gawthrop PJ, (2014) Does the motor system need intermittent control? Exercise and Sport Sciences Reviews 42: 117–25.
52. Watanabe RN, Magalhães FH, Elias LA, Chaud VM, Mello EM, et al. (2013) Influences of premotoneuronal command statistics on the scaling of motor output variability during isometric plantar flexion. Journal of Neurophysiology 110: 2592–606.
53. Mello EM, Magalhães FH, Kohn AF, (2013) Larger plantar flexion torque variability implies less stable balance in the young: an association affected by knee position. Human Movement Science 32: 1310–24.
54. Kavounoudias A, Roll R, Roll JP, (2001) Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. Journal of Physiology-London 532: 869–878.
55. Jacobs JV, Horak FB, (2007) Cortical control of postural responses. Journal of Neural Transmission 114: 1339–1348.
56. Proske U, Gandevia SC, (2012) The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiological Reviews 92: 1651–97.
57. Zehr EP, (2002) Considerations for use of the Hoffmann reflex in exercise studies. European Journal of Applied Physiology 86: 455–68.
58. Pierrot-Deseilligny E, Burke D (2012) The circuitry of the human spinal cord: Spinal and corticospinal mechanisms of movement. Cambridge: Cambridge University Press, 606 pp.
59. Aniss AM, Diener HC, Hore J, Gandevia SC, Burke D, (1990) Behavior of human muscle receptors when reliant on proprioceptive feedback during standing. Journal of Neurophysiology 64: 661–670.
60. Diener HC, Dichgans J, Guschlbauer B, Mau H, (1984) The significance of proprioception on postural stabilization as assessed by ischemia. Brain Research 296: 103–9.
61. Meyer PF, Oddsson LIE, De Luca CJ, (2004) The role of plantar cutaneous sensation in unperturbed stance. Experimental Brain Research 156: 505–12.
62. Duarte M, Harvey W, Zatsiorsky VM, (2000) Stabilographic analysis of unconstrained standing. Ergonomics 43: 1824–1839.
63. Markram H, (2006) The blue brain project. Nature Reviews Neuroscience 7: 153–160.
64. Raphael G, Tsianos GA, Loeb GE, (2010) Spinal-like regulator facilitates control of a two-degree-of-freedom wrist. Journal of Neuroscience 30: 9431–9444.
65. Eliasmith C, Stewart TC, Choo X, Bekolay T, DeWolf T, et al. (2012) A large-scale model of the functioning brain. Science 338: 1202–5.
66. Dideriksen JL, Negro F, Enoka RM, Farina D, (2012) Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness. Journal of Neurophysiology 107: 3357–3369.
67. Farina D, Negro F, Dideriksen JL, (2014) The effective neural drive to muscles is the common synaptic input to motor neurons. The Journal of Physiology 592: 3427–41.
68. Elias LA, Chaud VM, Kohn AF, (2012) Models of passive and active dendrite motoneuron pools and their differences in muscle force control. Journal of Computational Neuroscience 33: 515–531.
69. Elias LA, Kohn AF, (2013) Individual and collective properties of computationally efficient motoneuron models of types S and F with active dendrites. Neurocomputing 99: 521–533.
70. Bui TV, Grande G, Rose PK, (2008) Multiple modes of amplification of synaptic inhibition to motoneurons by persistent inward currents. Journal of Neurophysiology 99: 571–582.
71. Destexhe A, (1997) Conductance-based integrate-and-fire models. Neural Computation 9: 503–514.
72. Destexhe A, Mainen ZF, Sejnowski TJ, (1994) An efficient method for computing synaptic conductances based on a kinetic-model of receptor-binding. Neural Computation 6: 14–18.
73. Johnson MA, Polgar J, Weightman D, Appleton D, (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. Journal of the Neurological Sciences 18: 111–129.
74. McComas AJ, (1991) Invited review: motor unit estimation: methods, results, and present status. Muscle & Nerve 14: 585–597.
75. Cheng EJ, Brown IE, Loeb GE, (2000) Virtual muscle: a computational approach to understanding the effects of muscle properties on motor control. Journal of Neuroscience Methods 101: 117–130.
76. Thelen DG, (2003) Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. Journal of Biomechanical Engineering 125: 70–77.
77. de Vlugt E, de Groot JH, Wisman WH, Meskers CG, (2012) Clonus is explained from increased reflex gain and enlarged tissue viscoelasticity. Journal of Biomechanics 45: 148–155.
78. Bawa P, Stein RB, (1976) Frequency-response of human soleus muscle. Journal of Neurophysiology 39: 788–793.
79. Chaud VM, Elias LA, Watanabe RN, Kohn AF (2012) A simulation study of the effects of activation-dependent muscle stiffness on proprioceptive feedback and short-latency reflex. In: 4th IEEE RAS/EMBS International Conference on Biomedical Robotics and Biomechatronics. Rome: IEEE, pp. 133–138. doi:10.1109/BioRob.2012.6290871.
80. Watanabe RN, Elias LA, Kohn AF (2013) Low-frequency fluctuations of plantar flexion torque in force and position control tasks studied experimentally and by a neuromusculoskeletal model. In: 6th International IEEE/EMBS Conference on Neural Engineering (NER). IEEE, pp. 794–797. doi:10.1109/NER.2013.6696054.
81. Sartori M, Reggiani M, Farina D, Lloyd DG, (2012) EMG-driven forward-dynamic estimation of muscle force and joint moment about multiple degrees of freedom in the human lower extremity. PLoS One 7: e52618.
82. Arnold EM, Ward SR, Lieber RL, Delp SL, (2010) A model of the lower limb for analysis of human movement. Annals of Biomedical Engineering 38: 269–279.
83. Menegaldo LL, de Toledo Fleury A, Weber HI, (2004) Moment arms and musculotendon lengths estimation for a three-dimensional lower-limb model. Journal of Biomechanics 37: 1447–1453.
84. Mileusnic MP, Brown IE, Lan N, Loeb GE, (2006) Mathematical models of proprioceptors. I. Control and transduction in the muscle spindle. Journal of Neurophysiology 96: 1772–1788.
85. Lin CC, Crago PE, (2002) Neural and mechanical contributions to the stretch reflex: a model synthesis. Annals of Biomedical Engineering 30: 54–67.
86. Matthews PB, Stein RB, (1969) Regularity of primary and secondary muscle spindle afferent discharges. Journal of Physiology-London 202: 59–82.
87. Nardone A, Schieppati M, (1998) Medium-latency response to muscle stretch in human lower limb: estimation of conduction velocity of group II fibres and central delay. Neuroscience Letters 249: 29–32.
88. Banks RW, (2006) An allometric analysis of the number of muscle spindles in mammalian skeletal muscles. Journal of Anatomy 208: 753–768.
89. Burke D, Hagbarth KE, Skuse NF, (1978) Recruitment order of human spindle endings in isometric voluntary contractions. Journal of Physiology-London 285: 101–112.
90. Kearney RE, Hunter IW, (1982) Dynamics of human ankle stiffness: variation with displacement amplitude. Journal of Biomechanics 15: 753–756.
91. Hunter IW, Kearney RE, (1982) Dynamics of human ankle stiffness: variation with mean ankle torque. Journal of Biomechanics 15: 747–752.
92. Loeb GE, Brown IE, Cheng EJ, (1999) A hierarchical foundation for models of sensorimotor control. Experimental Brain Research 126: 1–18.