Somatosensory control of balance during locomotion in decerebrated cat

Journal of Neurophysiology

Volumn 107, Issue 8, 2012, Pages 2072-2082

  Musienko, Pavel ^a,b   Courtine, Gregoire ^b   Tibbs, Jameson E ^c   Kilimnik, Vyacheslav ^a   Savochin, Alexandr ^a   Garfinkel, Alan ^d   Roy, Roland R ^c   Reggie Edgerton, V ^c,d   Gerasimenko, Yury ^a,c  

^a PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epidural stimulation; Ground reaction forces; Lateral displacement

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BODY EQUILIBRIUM; BODY POSTURE; BRAIN FUNCTION; BRAIN STEM; CAT; CONTROLLED STUDY; DECEREBRATION; ELECTROMYOGRAM; HINDLIMB; KINEMATICS; MOTOR COORDINATION; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; SOMATOSENSORY STIMULATION; SPINAL CORD; SPINAL CORD STIMULATION; TAIL; TASK PERFORMANCE; TRUNK; WALKING; WEIGHT BEARING;

ANIMALS; CATS; DECEREBRATE STATE; EVOKED POTENTIALS, SOMATOSENSORY; HINDLIMB; LOCOMOTION; POSTURAL BALANCE; SOMATOSENSORY CORTEX;

EID: 84859783652     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00730.2011     Document Type: Article

References (67)

1. Armstrong DM. Supraspinal contributions to initiation and control of locomotion in the cat. Prog Neurobiol 26: 273-361, 1986.
2. Arshavsky YI, Gelfand IM, Orlovsky GN. The cerebellum and control of rhythmical movements. Trends Neurosci 6: 417-422, 1983.
3. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412: 84-95, 1987.
4. Barberini CL, Macpherson JM. Effect of head position on postural orientation and equilibrium. Exp Brain Res 122: 175-184, 1998.
5. Bard P, Macht MB. The behavior of chronically decerebrate cats. In: Neurological Basis of Behavior, edited by Wolstenholme GEW, O'Connor CM. London: Churchill, 1958, p. 55-71.
6. Beloozerova IN, Zelenin PV, Popova LB, Orlovsky GN, Grillner S, Deliagina TG. Postural control in the rabbit maintaining balance on the tilting platform. J Neurophysiol 90: 3783-3793, 2003.
7. Beloozerova IN, Sirota MG, Orlovsky GN, Deliagina TG. Activity of pyramidal tract neurons in the cat during postural corrections. J Neurophysiol 93: 1831-1844, 2005.
8. Bernstein N. The Co-ordination and Regulation of Movements. Oxford, UK: Pergamon, 1967.
9. Berthoz A, Pozzo T. Intermittent head stabilization during postural and locomotory tasks in humans. In: Posture and Gait: Development, Adaptation and Modulation, edited by Amblard B, Berthoz A, Clarac F. Amsterdam: Exerpta Medica, 1988, p. 189-198.
10. Bolton DA, Misiaszek JE. Contribution of hindpaw cutaneous inputs to the control of lateral stability during walking in the cat. J Neurophysiol 102: 1711-1724, 2009.
11. Boyle R. Vestibular control of reflex and voluntary head movement. Ann NY Acad Sci 942: 364-380, 2001.
12. Courtine G, Gerasimenko Y, van den Brand R, Yew A, Musienko P, Zhong H, Song B, Ao Y, Ichiyama RM, Lavrov I, Roy RR, Sofroniew MV, Edgerton VR. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12: 1333-1342, 2009.
13. Deliagina TG, Beloozerova IN, Popova LB, Sirota MG, Swadlow H, Grant G, Orlovsky GN. Role of different sensory inputs for maintenance of body posture in sitting rat and rabbit. Motor Control 4: 439-452, 2000.
14. Deliagina TG, Orlovsky GN, Zelenin PV, Beloozerova IN. Neural bases of postural control. Physiology 21: 216-225, 2006.
15. Di Fabio RP, Gerleman D, Soderberg GL, Melnick ME. An adaptable, multiple plate dynamometer and electromyograph for the study of quadruped postural responses. Electroencephalogr Clin Neurophysiol 54: 235-236, 1982.
16. Edgerton VR, Courtine G, Gerasimenko YP, Lavrov I, Ichiyama RM, Fong AJ, Cai LL, Otoshi CK, Tillakaratne NJ, Burdick JW, Roy RR. Training locomotor networks. Brain Res Rev 57: 241-254, 2008.
17. Fong AJ, Roy RR, Ichiyama RM, Lavrov I, Courtine G, Gerasimenko Y, Tai YC, Burdick J, Edgerton VR. Recovery of control of posture and locomotion after a spinal cord injury: solutions staring us in the face. Prog Brain Res 175: 393-418, 2009.
18. Gambaryan PP, Orlovskii GN, Protopopova TG, Severin FV, Shik ML. [The activity of muscles during different forms of locomotion in the cat and adaptive changes of locomotor organs in family Felidae.] Trury Zool Inst Acad Nauk (USSR) 48: 220-239, 1971.
19. Gaunt RA, Prochazka A, Mushahwar VK, Guevremont L, Ellaway PH. Intraspinal microstimulation excites multisegmental sensory afferents at lower stimulus levels than local alpha-motoneuron responses. J Neurophysiol 96: 2995-3005, 2006.
20. Gerasimenko YP, Lavrov IA, Bogacheva IN, Shcherbakova NA, Kucher VI, Musienko P. Formation of locomotor patterns in decerebrate cats in conditions of epidural stimulation of the spinal cord. Neurosci Behav Physiol 35: 291-298, 2005.
21. Gerasimenko YP, Lavrov IA, Courtine G, Ichiyama RM, Dy CJ, Zhong H, Roy RR, Edgerton VR. Spinal cord reflexes induced by epidural spinal cord stimulation in normal wake rats. J Neurosci Methods 157: 253-263, 2006.
22. Gerasimenko YP, Roy RR, Edgerton VR. Epidural stimulation: comparison of the spinal circuits that generate and control locomotion in rats, cats and humans. Exp Neurol 209: 417-425, 2008.
23. Gerasimenko Y, Musienko P, Bogacheva I, Moshonkina T, Savochin A, Lavrov I, Roy RR, Edgerton VR. Propriospinal bypass of the serotonergic system that can facilitate stepping. J Neurosci 29: 5681-5689, 2009.
24. Haour R, Massarino R, Massion J, Swett JE. A device used for study of postural reactions in the quadruped. Electroencephalogr Clin Neurophysiol 40: 427-431, 1976.
25. Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y, Ferreira C, Willhite A, Rejc E, Grossman RG, Edgerton VR. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 377: 1938-1947, 2011.
26. Hof AL. The "extrapolated center of mass" concept suggests a simple control of balance in walking. Hum Mov Sci 27: 112-125, 2008.
27. Honeycutt CF, Gottschall JS, Nichols TR. Electromyographic responses from the hindlimb muscles of the decerebrate cat to horizontal support surface perturbations. J Neurophysiol 101: 2751-2761, 2009.
28. Horak F, Macpherson J. Postural orientation and equilibrium. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am Physiol Soc, 1996, sect. 12, p. 255-292.
29. Iwahara T, Atsuta Y, Garcia-Rill E, Skinner R. Spinal cord stimulationinduced locomotion in adult cat. Brain Res Bull 28: 99-105, 1991.
30. Jankowska E, Jukes MGM, Lund S, Lundberg A. The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 70: 369-388, 1967a.
31. Jankowska E, Jukes MGM, Lund S, Lundberg A. The effect of DOPA on the spinal cord. 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol Scand 70: 389-402, 1967b.
32. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG. Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57: 183-191, 2008.
33. Karayannidou A, Zelenin PV, Orlovsky GN, Sirota MG, Beloozerova IN, Deliagina TG. Maintenance of lateral stability during standing and walking in the cat. J Neurophysiol 101: 8-19, 2009a.
34. Karayannidou A, Beloozerova IN, Zelenin PV, Stout EE, Sirota MG, Orlovsky GN, Deliagina TG. Activity of pyramidal tract neurons in the cat during standing and walking on an inclined plane. J Physiol 587: 3795-3811, 2009b.
35. Kazennikov OV, Selionov VA, Shik ML. On the bulbospinal locomotion column in the cat. In: Stance and Motion: Facts and Concepts. New York: Plenum, 1988, p. 123-131.
36. Kim SA, Heinze KG, Schwille P. Fluorescence correlation spectroscopy in living cells. Nat Methods 4: 963-973, 2007.
37. Kostyuk PG. [Integrative processes in the spinal cord.] In: Specific Physiology of the Nervous System. Leningrad: Nauka, 1983, p. 5-60.
38. Lockhart DB, Ting LH. Optimal sensorimotor transformations for balance. Nat Neurosci 10: 1329-1336, 2007.
39. Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res 514: 206-218, 1990.
40. Macpherson JM. Strategies that simplify the control of quadrupedal stance. I. Forces at the ground. J Neurophysiol 60: 204-217, 1988a.
41. Macpherson JM. Strategies that simplify the control of quadrupedal stance. II Electromyographic activity. J Neurophysiol 60: 218-231, 1988b.
42. Macpherson JM, Fung J, Jacobs R. Postural orientation, equilibrium, and the spinal cord. Adv Neurol 72: 227-232, 1997.
43. Magnus R. Korperstellun [Body posture]. Berlin: Springer, 1924.
44. Massion J. Postural control system. Curr Opin Neurobiol 4: 877-888, 1994.
45. Matsuyama K, Drew T. Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. II. Walking on an inclined plane. J Neurophysiol 84: 2257-2276, 2000.
46. Misiaszek JE. Control of frontal plane motion of the hindlimbs in the unrestrained walking cat. J Neurophysiol 96: 1816-1828, 2006a.
47. Misiaszek JE. Neural control of walking balance: if falling then react else continue. Exerc Sport Sci Rev 34: 128-134, 2006b.
48. Moor SP, Rushmer DS, Windus SL, Nashner LM. Human automatic postural responses: responses to horizontal perturbations of stance in multiple directions. Exp Brain Res 73: 648-658, 1988.
49. Mori S, Kawahara K, Sakamoto T. Supraspinal aspects of locomotion in the mesencephalic cat. In: Neural Control, edited by Roberts A, Roberts BL. Cambridge, UK: Cambridge Univ. Press, 1983, p. 445-468.
50. Mori S. Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats. Prog Neurobiol 28: 161-196, 1987.
51. Musienko PE, Bogacheva IN, Gerasimenko YP. Significance of peripheral feedback in the generation of stepping movements during epidural stimulation of the spinal cord. Neurosci Behav Physiol 37: 181-190, 2007.
52. Musienko PE, Zelenin PV, Lylalka VF, Orlovsky GN, Deliagina TG. Postural performance in decerebrated rabbit. Behav Brain Res 190: 124-134, 2008.
53. Musienko P, Edgerton VR, Zelenkova N, Courtine G, Gerasimenko Y. Decerebrated cats show somatosensory-driven postural reactions during locomotion facilitated by epidural stimulation. Soc Neurosci Abstr 2009: 80.6, 2009a.
54. Musienko PE, Pavlova NV, Selionov VA, Gerasimenko IuP. [Locomotion induced by epidural stimulation in decerebrate cat after spinal cord injury.] Biofizika 54: 293-300, 2009b.
55. Musienko P, van den Brand R, Maerzendorfer O, Larmagnac A, Courtine G. Combinatory electrical and pharmacological neuroprosthetic interfaces to regain motor function after spinal cord injury. IEEE Trans Biomed Eng 56: 2707-2711, 2009c.
56. Musienko PE, Zelenin PV, Orlovsky GN, Deliagina TG. Facilitation of postural limb reflexes with epidural stimulation in spinal rabbits. J Neurophysiol 103: 1080-1092, 2010.
57. Musienko P, van den Brand R, Maerzendorfer O, Roy RR, Gerasimenko Y, Edgerton VR, Courtine G. Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J Neurosci 31: 9262-9278, 2011a.
58. Musienko P, Heutschi J, Friedli L, van den Brand R, Courtine G. Multi-system neurorehabilitative strategies to restore motor functions following severe spinal cord injury. Exp Neurol (September 7, 2011).doi: 10.1016/j.expneurol.2011.08.025, 2011b.
59. Rasmussen S, Chan AK, Goslow GE Jr. The cat step cycle: electromyographic patterns for hindlimb muscles during posture and unrestrained locomotion. J Morphol 155: 253-269, 1978.
60. Rattay F, Minassian K, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord. 2. Quantitative analysis by computer modeling. Spinal Cord 38: 473-489, 2000.
61. Roberts TDM. Neurophysiology of Postural Mechanisms. London: Butterworths, 1978.
62. Sherrington C. Flexion-reflex of the limb, crossed extension reflex, and reflex stepping and standing. J Physiol 40: 28-121, 1910.
63. Shik ML, Severin FV, Orlovsky GN. Control of walking and running by means of electrical stimulation of the mid-brain. Biofizika 11: 756-765, 1966.
64. Shik ML, Orlovsky GN. Neurophysiology of locomotor automatism. Physiol Rev 56: 465-501, 1976.
65. Silverman J, Garnett NL, Giszter SF, Heckman CJ 2nd, Kulpa-Eddy JA, Lemay MA, Perry CK, Pinter M. Decerebrate mammalian preparations: unalleviated or fully alleviated pain? A review and opinion. Contemp Top Lab Anim Sci 44: 34-36, 2005.
66. Whelan PJ. Control of locomotion in the decerebrate cat. Prog Neurobiol 49: 481-515, 1996.
67. Zelenin PV, Beloozerova IN, Sirota MG, Orlovsky GN, Deliagina TG. Activity of red nucleus neurons in the cat during postural corrections. J Neurosci 30: 14533-14542, 2010.