Novel mechanism for hyperreflexia and spasticity

Progress in Brain Research

Volumn 188, Issue , 2011, Pages 167-180

  Yates, C ^a,b   Garrison, K ^a,b   Reese, N B ^b   Charlesworth, A ^a   Garcia Rill, E ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF CENTRAL ARKANSAS   (United States)

Author keywords

Electrical coupling; Gap junctions; H reflex; Hyperreflexia; Spasticity; Spinal cord injury; Stretch reflex

Indexed keywords

CONNEXIN 36; GAP JUNCTION PROTEIN;

ALPHA NERVE FIBER; BOOK; DEPRESSION; ELECTRICAL SYNAPSE; ELECTROGASTROGRAPHY; EXERCISE; HOFFMANN REFLEX; HUMAN; HYPERREFLEXIA; MYOTATIC REFLEX; NONHUMAN; PASSIVE MOVEMENT; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SPASTICITY; SPINAL CORD INJURY; ANIMAL; MOVEMENT (PHYSIOLOGY); PATHOLOGICAL REFLEX; PATHOLOGY; PATHOPHYSIOLOGY; PERIODICITY; PHYSIOLOGY; REVIEW;

ANIMALS; H-REFLEX; HUMANS; MOVEMENT; MUSCLE SPASTICITY; PERIODICITY; REFLEX, ABNORMAL; REFLEX, STRETCH; SPINAL CORD INJURIES;

EID: 79951658744     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-53825-3.00016-4     Document Type: Chapter

References (97)

1. Angel R.W., Hofmann W.W. The H reflex in normal, spastic, and rigid subjects. Archives of Neurology 1963, 9:591-596.
2. Arfaj A., Yates C., Reese N.B., Ishida K., Skinner R.D., Garcia-Rill E. Changes in the H-reflex after spinal cord injury: A longitudinal study in awake rats. Neuroscience-Abstract 2007, 33:405-422.
3. Atsuta Y., Abraham P., Iwahara T., Garcia-Rill E., Skinner R.D. Control of locomotion in vitro: II. Chemical stimulation. Somatosensory & Motor Research 1991, 8:55-63.
4. Atsuta Y., Garcia-Rill E., Skinner R.D. Electrically induced locomotion in the in vitro brainstem-spinal cord preparation. Brain Research 1988, 470:309-312.
5. Ballon J.S., Feifel D. A systematic review of modafinil: Potential clinical uses and mechanisms of action. The Journal of Clinical Psychiatry 2006, 67:554-566.
6. Bennett D.J., Gorassini M., Fouad K., Sanelli L., Han Y., Cheng J. Spasticity in rats with sacral spinal cord injury. Journal of Neurotrauma 1999, 16:69-84.
7. Bennett D.J., Hultborn H., Fedirchuk B., Gorassini M. Short-term plasticity in hindlimb motoneurons of decerebrate cats. Journal of Neurophysiology 1998, 80:2038-2045.
8. Bennett D.J., Li Y., Harvey P.J., Gorassini M. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. Journal of Neurophysiology 2001, 86:1972-1982.
9. Blatow M., Rozov A., Katona I., Hormuzdi S.G., Meyer A.H., Whittington M.A., et al. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 2003, 38:805-817.
10. Bose P., Parmer R., Thompson F.J. Velocity-dependent ankle torque in rats after contusion injury of the midthoracic spinal cord: Time course. Journal of Neurotrauma 2002, 19:1231-1249.
11. Bou-Flores C., Berger A.J. Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. Journal of Neurophysiology 2001, 85:1543-1551.
12. Bradley N.S. Animal models offer the opportunity to acquire a new perspective on motor development. Physical Therapy 1990, 70:776-787.
13. Calancie B., Broton J.G., Klose K.J., Traad M., Difini J., Ayyar D.R. Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalography and Clinical Neurophysiology 1993, 89:177-186.
14. Calancie B., Molano M.R., Broton J.G. Interlimb reflexes and synaptic plasticity become evident months after human spinal cord injury. Brain 2002, 125:1150-1161.
15. Chen X.Y., Feng-Chen K.C., Chen L., Stark D.M., Wolpaw J.R. Short-Term and medium-term effects of spinal cord tract transections on soleus H-reflex in freely moving rats. Journal of Neurotrauma 2001, 18:313-327.
16. Christie M.J., Williams J.T., North R.A. Electrical coupling synchronizes subthreshold activity in locus coeruleus neurons in vitro from neonatal rats. The Journal of Neuroscience 1989, 9:3584-3589.
17. Cifra A., Nani F., Sharifullina E., Nistri A. A repertoire of rhythmic bursting produced by hypoglossal motoneurons in physiological and pathological conditions. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 2009, 364:2493-2500.
18. Condorelli D.F., Parenti R., Spinella F., Trovato Salinaro A., Belluardo N., Cardile V., et al. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. The European Journal of Neuroscience 1998, 10:1202-1208.
19. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Annual Review of Neuroscience 2004, 27:393-418.
20. Crone C., Hultborn H., Kiehn O., Mazieres L., Wigstrom H. Maintained changes in motoneuronal excitability by short-lasting synaptic inputs in the decerebrate cat. Journal de Physiologie 1988, 405:321-343.
21. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 2001, 31:477-485.
22. Dietz V., Quintern J., Berger W. Electrophysiological studies of gait in spasticity and rigidity. Evidence that altered mechanical properties of muscle contribute to hypertonia. Brain 1981, 104:431-449.
23. Eken T., Hultborn H., Kiehn O. Possible functions of transmitter-controlled plateau potentials in alpha motoneurones. Progress in Brain Research 1989, 80:257-267.
24. Elsen F.P., Shields E.J., Roe M.T., Vandam R.J., Kelty J.D. Carbenoxolone induced depression of rhythmogenesis in the pre-Botzinger Complex. BMC Neuroscience 2008, 9:46.
25. Enriquez-Denton M., Morita H., Christensen L.O., Petersen N., Sinkjaer T., Nielsen J.B. Interaction between peripheral afferent activity and presynaptic inhibition of ia afferents in the cat. Journal of Neurophysiology 2002, 88:1664-1674.
26. Faist M., Mazevet D., Dietz V., Pierrot-Deseilligny E. A quantitative assessment of presynaptic inhibition of Ia afferents in spastics. Differences in hemiplegics and paraplegics. Brain 1994, 117(Pt. 6):1449-1455.
27. Fawcett J.W. Overcoming inhibition in the damaged spinal cord. Journal of Neurotrauma 2006, 23:371-383.
28. Friedman D., Strowbridge B.W. Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. Journal of Neurophysiology 2003, 89:2601-2610.
29. Fulton B.P., Miledi R., Takahashi T. Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proceedings of the Royal Society of London. Series B: Biological Sciences 1980, 208:115-120.
30. Garcia-Rill E. The pedunculopontine nucleus. Progress in Neurobiology 1991, 36:363-389.
31. Garcia-Rill E., Heister D.S., Ye M., Charlesworth A., Hayar A. Electrical coupling: Novel mechanism for sleep-wake control. Sleep 2007, 30:1405-1414.
32. Garcia-Rill E., Skinner R.D. Modulation of rhythmic function in the posterior midbrain. Neuroscience 1988, 27:639-654.
33. Garcia-Rill E., Skinner R.D., Fitzgerald J.A. Chemical activation of the mesencephalic locomotor region. Brain Research 1985, 330:43-54.
34. Grey M.J., Klinge K., Crone C., Lorentzen J., Biering-Sorensen F., Ravnborg M., et al. Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Experimental Brain Research 2008, 185:189-197.
35. Heister D.S., Hayar A., Charlesworth A., Yates C., Zhou Y.H., Garcia-Rill E. Evidence for electrical coupling in the SubCoeruleus (SubC) nucleus. Journal of Neurophysiology 2007, 97:3142-3147.
36. Hewitt A., Barrie R., Graham M., Bogus K., Leiter J.C., Erlichman J.S. Ventilatory effects of gap junction blockade in the RTN in awake rats. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2004, 287:R1407-R1418.
37. Hinckley C.A., Ziskind-Conhaim L. Electrical coupling between locomotor-related excitatory interneurons in the mammalian spinal cord. The Journal of Neuroscience 2006, 26:8477-8483.
38. Honma S., De S., Li D., Shuler C.F., Turman J.E. Developmental regulation of connexins 26, 32, 36, and 43 in trigeminal neurons. Synapse 2004, 52:258-271.
39. Hornby T.G., Kahn J.H., Wu M., Schmit B.D. Temporal facilitation of spastic stretch reflexes following human spinal cord injury. Journal de Physiologie 2006, 571:593-604.
40. Hornby T.G., Rymer W.Z., Benz E.N., Schmit B.D. Windup of flexion reflexes in chronic human spinal cord injury: A marker for neuronal plateau potentials? Journal of Neurophysiology 2003, 89:416-426.
41. Hounsgaard J., Hultborn H., Jespersen B., Kiehn O. Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. The Journal of Physiology 1988, 405:345-367.
42. Hultborn H. Changes in neuronal properties and spinal reflexes during development of spasticity following spinal cord lesions and stroke: Studies in animal models and patients. Journal of Rehabilitation Medicine 2003, 46-55.
43. Hurst D., Cedrone N. Modafinil for drooling in cerebral palsy. Journal of Child Neurology 2006, 21:112-114.
44. Hurst D.L., Lajara-Nanson W.A., Lance-Fish M.E. Walking with modafinil and its use in diplegic cerebral palsy: Retrospective review. Journal of Child Neurology 2006, 21:294-297.
45. Ishikawa K., Ott K., Porter R.W., Stuart D. Low frequency depression of the H wave in normal and spinal man. Experimental Neurology 1966, 15:140-156.
46. Ju M.S., Chen J.J., Lee H.M., Lin T.S., Lin C.C., Huang Y.Z. Time-course analysis of stretch reflexes in hemiparetic subjects using an on-line spasticity measurement system. Journal of Electromyography and Kinesiology 2000, 10:1-14.
47. Kiehn O., Tresch M.C. Gap junctions and motor behavior. Trends in Neurosciences 2002, 25:108-115.
48. Kiser T.S., Reese N.B., Maresh T., Hearn S., Yates C., Skinner R.D., et al. Use of a motorized bicycle exercise trainer to normalize frequency-dependent habituation of the H-reflex in spinal cord injury. The Journal of Spinal Cord Medicine 2005, 28:241-245.
49. Kistler W.M., De Jeu M.T., Elgersma Y., Van Der Giessen R.S., Hensbroek R., Luo C., et al. Analysis of Cx36 knockout does not support tenet that olivary gap junctions are required for complex spike synchronization and normal motor performance. Annals of the New York Academy of Sciences 2002, 978:391-404.
50. Kita M., Goodkin D.E. Drugs used to treat spasticity. Drugs 2000, 59:487-495.
51. Kitzman P. Alteration in axial motoneuronal morphology in the spinal cord injured spastic rat. Experimental Neurology 2005, 192:100-108.
52. Kuhn R.A. Functional capacity of the isolated human spinal cord. Brain 1950, 73:1-51.
53. Lance J.W. Symposium synopsis. Spasticity: Disordered motor control 1980, 485-494. Year Book, Chicago. R.G. Feldman, R.R. Young, W.P. Koella (Eds.).
54. Landau W.M., Clare M.H. Fusimotor Function. Vi. H Reflex, Tendon Jerk, and Reinforcement in Hemiplegia. Archives of Neurology 1964, 10:128-134.
55. Leznik E., Llinas R. Role of gap junctions in synchronized neuronal oscillations in the inferior olive. Journal of Neurophysiology 2005, 94:2447-2456.
56. Li Y., Bennett D.J. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. Journal of Neurophysiology 2003, 90:857-869.
57. Li W.C., Roberts A., Soffe S.R. Locomotor rhythm maintenance: Electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles. Journal de Physiologie 2009, 587:1677-1693.
58. Little J.W., Ditunno J.F., Stiens S.A., Harris R.M. Incomplete spinal cord injury: Neuronal mechanisms of motor recovery and hyperreflexia. Archives of Physical Medicine and Rehabilitation 1999, 80:587-599.
59. Little J.W., Halar E.M. H-reflex changes following spinal cord injury. Archives of Physical Medicine and Rehabilitation 1985, 66:19-22.
60. Long M.A., Deans M.R., Paul D.L., Connors B.W. Rhythmicity without synchrony in the electrically uncoupled inferior olive. The Journal of Neuroscience 2002, 22:10898-10905.
61. Magladery J.W., Teasdall R.D., Park A.M., Languth H.W. Electrophysiological studies of reflex activity in patients with lesions of the nervous system. I. A comparison of spinal motoneurone excitability following afferent nerve volleys in normal persons and patients with upper motor neurone lesions. Bulletin of the Johns Hopkins Hospital 1952, 91:219-244. (passim).
62. Meinck H.M. Occurrence of the H reflex and the F wave in the rat. Electroencephalography and Clinical Neurophysiology 1976, 41:530-533.
63. Milanov I. Examination of the segmental pathophysiological mechanisms of spasticity. Electromyography and Clinical Neurophysiology 1994, 34:73-79.
64. Morita H., Petersen N., Christensen L.O., Sinkjaer T., Nielsen J. Sensitivity of H-reflexes and stretch reflexes to presynaptic inhibition in humans. Journal of Neurophysiology 1998, 80:610-620.
65. Nakazawa K., Kawashima N., Akai M. Enhanced stretch reflex excitability of the soleus muscle in persons with incomplete rather than complete chronic spinal cord injury. Archives of Physical Medicine and Rehabilitation 2006, 87:71-75.
66. Nielsen J., Petersen N., Crone C. Changes in transmission across synapses of Ia afferents in spastic patients. Brain 1995, 118(Pt. 4):995-1004.
67. Olsen P.Z., Diamantopoulos E. Excitability of spinal motor neurones in normal subjects and patients with spasticity, Parkinsonian rigidity, and cerebellar hypotonia. Journal of Neurology, Neurosurgery and Psychiatry 1967, 30:325-331.
68. Parisian K., Wages P., Smith A., Jarosz J., Hewitt A., Leiter J.C., et al. Ventilatory effects of gap junction blockade in the NTS in awake rats. Respiratory Physiology & Neurobiology 2004, 142:127-143.
69. Pierrot-Deseilligny E. Electrophysiological assessment of the spinal mechanisms underlying spasticity. Electroencephalography and Clinical Neurophysiology. Supplement 1990, 41:64-273.
70. Placantonakis D.G., Bukovsky A.A., Zeng X.H., Kiem H.P., Welsh J.P. Fundamental role of inferior olive connexin 36 in muscle coherence during tremor. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:7164-7169.
71. Powers R.K., Rymer W.Z. Effects of acute dorsal spinal hemisection on motoneuron discharge in the medial gastrocnemius of the decerebrate cat. Journal of Neurophysiology 1988, 59:1540-1556.
72. Reese N.B., Skinner R.D., Mitchell D., Yates C., Barnes C.N., Kiser T.S., et al. Restoration of frequency-dependent depression of the H-reflex by passive exercise in spinal rats. Spinal Cord 2006, 44:28-34.
73. Rekling J.C., Feldman J.L. Bidirectional electrical coupling between inspiratory motoneurons in the newborn mouse nucleus ambiguus. Journal of Neurophysiology 1997, 78:3508-3510.
74. Roopun A.K., Middleton S.J., Cunningham M.O., LeBeau F.E., Bibbig A., Whittington M.A., et al. A beta2-frequency (20-30Hz) oscillation in nonsynaptic networks of somatosensory cortex. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:15646-15650.
75. Schindler-Ivens S., Shields R.K. Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Experimental Brain Research 2000, 133:233-241.
76. Schindler-Ivens S.M., Shields R.K. Soleus H-reflex recruitment is not altered in persons with chronic spinal cord injury. Archives of Physical Medicine and Rehabilitation 2004, 85:840-847.
77. Schmit B.D., Benz E.N., Rymer W.Z. Afferent mechanisms for the reflex response to imposed ankle movement in chronic spinal cord injury. Experimental Brain Research 2002, 145:40-49.
78. Schmit B.D., Dhaher Y., Dewald J.P., Rymer W.Z. Reflex torque response to movement of the spastic elbow: Theoretical analyses and implications for quantification of spasticity. Annals of Biomedical Engineering 1999, 27:815-829.
79. Sinfield J.L., Collins D.R. Induction of synchronous oscillatory activity in the rat lateral amygdala in vitro is dependent on gap junction activity. The European Journal of Neuroscience 2006, 24:3091-3095.
80. Sinkjaer T., Toft E., Larsen K., Andreassen S., Hansen H.J. Non-reflex and reflex mediated ankle joint stiffness in multiple sclerosis patients with spasticity. Muscle & Nerve 1993, 16:69-76.
81. Skinner R.D., Houle J.D., Reese N.B., Berry C.L., Garcia-Rill E. Effects of exercise and fetal spinal cord implants on the H-reflex in chronically spinalized adult rats. Brain Research 1996, 729:127-131.
82. Soderberg G.L., Knutson L.M. A guide for use and interpretation of kinesiologic electromyographic data. Physical Therapy 2000, 80:485-498.
83. Stelzner D.J., Ershler W.B., Weber E.D. Effects of spinal transection in neonatal and weanling rats: Survival of function. Experimental Neurology 1975, 46:156-177.
84. Thompson F.J., Browd C.R., Carvalho P.M., Hsiao J. Velocity-dependent ankle torque in the normal rat. NeuroReport 1996, 7:2273-2276.
85. Thompson F.J., Parmer R., Reier P.J., Wang D.C., Bose P. Scientific basis of spasticity: Insights from a laboratory model. Journal of Child Neurology 2001, 16:2-9.
86. Thompson F.J., Reier P.J., Lucas C.C., Parmer R. Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. Journal of Neurophysiology 1992, 68:1473-1486.
87. Traub R.D., Pais I., Bibbig A., LeBeau F.E., Buhl E.H., Hormuzdi S.G., et al. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:1370-1374.
88. Tresch M.C., Kiehn O. Motor coordination without action potentials in the mammalian spinal cord. Nature Neuroscience 2000, 3:593-599.
89. Urbano F.J., Leznik E., Llinas R.R. Modafinil enhances thalamocortical activity by increasing neuronal electrotonic coupling. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:12554-12559.
90. Verdier D., Lund J.P., Kolta A. Synaptic inputs to trigeminal primary afferent neurons cause firing and modulate intrinsic oscillatory activity. Journal of Neurophysiology 2004, 92:2444-2455.
91. Walton K.D., Navarrete R. Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. Journal de Physiologie 1991, 433:283-305.
92. Wenner P., O'Donovan M.J. Mechanisms that initiate spontaneous network activity in the developing chick spinal cord. Journal of Neurophysiology 2001, 86:1481-1498.
93. Woods A.J., Mennemeier M., Garcia-Rill E., Meythaler J., Mark V.W., Jewel G.R., et al. Bias in magnitude estimation following left hemisphere injury. Neuropsychologia 2006, 44:1406-1412.
94. Yablon S.A., Stokic D.S. Neurophysiologic evaluation of spastic hypertonia: Implications for management of the patient with the intrathecal baclofen pump. American Journal of Physical Medicine & Rehabilitation 2004, 83:S10-S18.
95. Yates C., Charlesworth A., Allen S.R., Reese N.B., Skinner R.D., Garcia-Rill E. The onset of hyperreflexia in the rat following complete spinal cord transection. Spinal Cord 2008, 46:798-803.
96. Yates C.C., Charlesworth A., Reese N.B., Ishida K., Skinner R.D., Garcia-Rill E. Modafinil normalized hyperreflexia after spinal transection in adult rats. Spinal Cord 2009, 47:481-485.
97. Yates C.C., Charlesworth A., Reese N.B., Skinner R.D., Garcia-Rill E. The effects of passive exercise therapy initiated prior to or after the development of hyperreflexia following spinal transection. Experimental Neurology 2008, 213:405-409.