Selective effects of baclofen on use-dependent modulation of GABAB inhibition after tetraplegia

Journal of Neuroscience

Volumn 33, Issue 31, 2013, Pages 12898-12907

  Barry, Melissa D ^a   Bunday, Karen L ^a   Chen, Robert ^b   Perez, Monica A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; BACLOFEN;

ADULT; ARTICLE; BRAIN CORTEX; CERVICAL SPINAL CORD INJURY; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGY; EVOKED MUSCLE RESPONSE; FEMALE; HUMAN; LATENT PERIOD; MALE; MOTOR DYSFUNCTION; NERVE CELL INHIBITION; NERVE CELL NETWORK; NEUROMODULATION; PRIORITY JOURNAL; QUADRIPLEGIA; SPASTICITY; SPIKE WAVE; SPINAL NERVE; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; ANALYSIS OF VARIANCE; ANTIMANIC AGENTS; BACLOFEN; CASE-CONTROL STUDIES; CORTICAL SPREADING DEPRESSION; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FINGERS; GABA-B RECEPTOR AGONISTS; HUMANS; LITHIUM CHLORIDE; MALE; MIDDLE AGED; MOTOR CORTEX; NEURAL INHIBITION; QUADRIPLEGIA; SPINAL CORD INJURIES;

EID: 84880763753     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1552-13.2013     Document Type: Article

References (67)

1. Aydin G, Tomruk S, Keleş I, Demir SO, Orkun S (2005) Transcutaneous electrical nerve stimulation versus baclofen in spasticity: clinical and electrophysiologic comparison. Am J Phys Med Rehabil 84:584-592. CrossRef Medline
2. Aymard C, Katz R, Lafitte C, Lo E, Pénicaud A, Pradat-Diehl P, Raoul S (2000) Presynaptic inhibition and homosynaptic depression: a comparison between lower and upper limbs in normal human subjects and patients with hemiplegia. Brain 123:1688-1702. CrossRef Medline
3. Azouvi P, Mane M, Thiebaut JB, Denys P, Remy-Neris O, Bussel B (1996) Intrathecal baclofen administration for control of severe spinal spasticity: functional improvement and long-term follow-up. Arch Phys Med Rehabil 77:35-39. CrossRef Medline
4. Beres-Jones JA, Johnson TD, Harkema SJ (2003) Clonus after human spinal cord injury cannot be attributed solely to recurrent muscle-tendon stretch. Exp Brain Res 149:222-236. Medline
5. Bunday KL, Perez MA (2012) Impaired crossed facilitation of the corticospinal pathway after cervical spinal cord injury. J Neurophysiol 107: 2901-2911. CrossRef Medline
6. Burke D, Andrews CJ, Knowles L (1971) The action of a GABA derivative in human spasticity. J Neurol Sci 14:199-208. CrossRef Medline
7. Burke D, Hicks R, Gandevia SC, Stephen J, Woodforth I, CrawfordM (1993) Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol 470:383-393. Medline
8. Butler JE, Petersen NC, Herbert RD, Gandevia SC, Taylor JL (2012) Origin of the low-levelEMGduring the silent period following transcranial magnetic stimulation. Clin Neurophysiol 123:1409-1414. CrossRef Medline
9. Calancie B, Broton JG, Klose KJ, Traad M, Difini J, Ayyar DR (1993) Evidence that alterations in presynaptic inhibition contribute to segmental hypo-and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol 89:177-186. CrossRef Medline
10. Chen R, Lozano AM, Ashby P (1999) Mechanism of the silent period following transcranial magnetic stimulation: evidence from epidural recordings. Exp Brain Res 128:539-542. CrossRef Medline
11. Curtis DR, Gynther BD, Lacey G, Beattie DT (1997) Baclofen: reduction of presynaptic calcium influx in the cat spinal cord in vivo. Exp Brain Res 113:520-533. CrossRef Medline
12. D'Amico JM, Li Y, Bennett DJ, Gorassini MA (2013) Reduction of spinal sensory transmission by facilitation of 5HT1 receptors in non-injured and spinal cord injured humans. J Neurophysiol 109:1485-1493. CrossRef Medline
13. DeiszRA (1999) GABA(B) receptor-mediated effects in human and rat neocortical neurones in vitro. Neuropharmacology 38:1755-1766. CrossRef Medline
14. Diaz-Ruiz A, Salgado-Ceballos H, Montes S, Maldonado V, Tristan L, Alcaraz-Zubeldia M, Ríos C (2007) Acute alterations of glutamate, glutamine, GABA, and other amino acids after spinal cord contusion in rats. Neurochem Res 32:57-63. CrossRef Medline
15. Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109:397-401. CrossRef Medline
16. Di Lazzaro V, Oliviero A, Mazzone P, Pilato F, Saturno E, Insola A, Visocchi M, Colosimo C, Tonali PA, Rothwell JC (2002) Direct demonstration of long latency cortico-cortical inhibition in normal subjects and in a patient with vascular parkinsonism. Clin Neurophysiol 113:1673-1679. CrossRef Medline
17. Domingo A, Al-Yahya AA, Asiri Y, Eng JJ, Lam T (2012) Asystematic review of the effects of pharmacological agents on walking function in people with spinal cord injury. J Neurotrauma 29:865-879. CrossRef Medline
18. Faist M, Mazevet D, Dietz V, Pierrot-Deseilligny E (1994) A quantitative assessment of presynaptic inhibition of Ia afferents in spastics: differences in hemiplegics and paraplegics. Brain 117:1449-1455. CrossRef Medline
19. Freund P, Rothwell J, Craggs M, Thompson AJ, Bestmann S (2011) Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury. Eur J Neurosci 34:1839-1846. CrossRef Medline
20. Fuhr P, Agostino R, HallettM (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257-262. CrossRef Medline
21. Hammond G, Vallence AM (2007) Modulation of long-interval intracortical inhibition and the silent period by voluntary contraction. Brain Res 1158:63-70. CrossRef Medline
22. Hornby TG, Heckman CJ, Harvey RL, Rymer WZ (2004) Changes in voluntary torque and electromyographic activity following oral baclofen. Muscle Nerve 30:784-795. CrossRef Medline
23. Jiménez I, Rudomin P, Enriquez M (1991) Differential effects of (-)-baclofen on Ia and descending monosynaptic EPSPs. Exp Brain Res 85: 103-113. Medline
24. Kato M, Waldmann U, Murakami S (1978) Effects of baclofen on spinal neurones of cats. Neuropharmacology 17:827-833. CrossRef Medline
25. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501-519. Medline
26. Kumru H, Kofler M (2012) Effect of spinal cord injury and of intrathecal baclofen on brainstem reflexes. Clin Neurophysiol 123:45-53. CrossRef Medline
27. Latash ML, Penn RD, Corcos DM, Gottlieb GL (1989) Short-term effects of intrathecal baclofen in spasticity. Exp Neurol 103:165-172. CrossRef Medline
28. Li Y, Li X, Harvey PJ, Bennett DJ (2004) Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92:2694-2703. CrossRef Medline
29. Marino RJ, Barros T, Biering-Sorensen F, Burns SP, Donovan WH, Graves DE, Haak M, Hudson LM, Priebe MM (2003) International standards for neurological classification of spinal cord injury. J Spinal Cord Med 26:50-56. Medline
30. McDonnell MN, Orekhov Y, Ziemann U (2006) The role of GABAB receptors in intracortical inhibition in the human motor cortex. Exp Brain Res 173:86-93. CrossRef Medline
31. McDonnell MN, Orekhov Y, Ziemann U (2007) Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen. Exp Brain Res 180:181-186. CrossRef Medline
32. McNeil CJ, Martin PG, Gandevia SC, Taylor JL (2009) The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J Physiol 587:5601-5612. CrossRef Medline
33. McNeil CJ, Martin PG, Gandevia SC, Taylor JL (2011) Long-interval intracortical inhibition in a human hand muscle. Exp Brain Res 209:287-297. CrossRef Medline
34. Misgeld U, Bijak M, Jarolimek W (1995) A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol 46:423-462. CrossRef Medline
35. Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1997) Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498:817-823. Medline
36. Ohliger-Frerking P, Wiebe SP, Stäubli U, Frerking M (2003) GABA(B) receptor-mediated presynaptic inhibition has history-dependent effects on synaptic transmission during physiologically relevant spike trains. J Neurosci 23:4809-4814. Medline
37. Orsnes G, Crone C, Krarup C, Petersen N, Nielsen J (2000) The effect of baclofen on the transmission in spinal pathways in spastic multiple sclerosis patients. Clin Neurophysiol 111:1372-1379. CrossRef Medline
38. Palmer DT, Horn LJ, Harmon RL (1998) Botulinum toxin treatment of lumbrical spasticity: a brief report. Am J Phys Med Rehabil 77:348-350. CrossRef Medline
39. Penn RD, Savoy SM, Corcos D, Latash M, Gottlieb G, Parke B, Kroin JS (1989) Intrathecal baclofen for severe spinal spasticity. N Engl J Med 320:1517-1521. CrossRef Medline
40. Pierrot-Deseilligny E, Burke D (2005) Propriospinal relay for descending motor commands. In: The circuitry of the human spinal cord, pp 452-510. New York: Cambridge UP.
41. Price GW, Wilkin GP, Turnbull MJ, Bowery NG (1984) Are baclofensensitive GABAB receptors present on primary afferent terminals of the spinal cord? Nature 307:71-74. CrossRef Medline
42. Price GW, Kelly JS, Bowery NG (1987) The location of GABAB receptors binding sites in mammalian spinal cord. Synapse 1:530-538. CrossRef Medline
43. Quevedo J, Eguibar JR, Jiménez I, Rudomin P (1992) Differential action of (-)-baclofen on the primary afferent depolarization produced by segmental and descending inputs. Exp Brain Res 91:29-45. CrossRef Medline
44. Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M, Perez MA, Ragert P, Rothwell JC, Cohen LG (2008) Contribution of transcranial magnetic stimulation to the understanding of cortical mech-anisms involved in motor control. J Physiol 586:325-351. CrossRef Medline
45. Rösche J (2002) Treatment of spasticity. Spinal Cord 40:261-262. CrossRef Medline
46. Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74:113-122. CrossRef Medline
47. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:97-103. Medline
48. Roy FD, Zewdie ET, Gorassini MA (2011) Short-interval intracortical inhibition with incomplete spinal cord injury. Clin Neurophysiol 122: 1387-1395. CrossRef Medline
49. Roy RR, Edgerton VR (2012) Neurobiological perspective of spasticity as occurs after a spinal cord injury. Exp Neurol 235:116-1122. CrossRef Medline
50. Rudomin P, Schmidt RF (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129:1-37. CrossRef Medline
51. Sadlaoud K, Tazerart S, Brocard C, Jean-Xavier C, Portalier P, Brocard F, Vinay L, Bras H (2010) Differential plasticity of the GABAergic and glycinergic synaptic transmission to rat lumbar motoneurons after spinal cord injury. J Neurosci 30:3358-3369. CrossRef Medline
52. Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997) Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp Brain Res 113:24-32. CrossRef Medline
53. Saturno E, Bonato C, Miniussi C, Lazzaro V, Callea L (2008) Motor cortex changes in spinal cord injury: a TMS study. Neurol Res 30:1084-1085. CrossRef Medline
54. Shimizu T, Hino T, Komori T, Hirai S (2000) Loss of the muscle silent period evoked by transcranial magnetic stimulation of the motor cortex in patients with cervical cord lesions. Neurosci Lett 286:199-202. CrossRef Medline
55. Siebner HR, Dressnandt J, Auer C, Conrad B (1998) Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21: 1209-1212. CrossRef Medline
56. Stuart GJ, Redman SJ (1992) The role of GABAA and GABAB receptors in presynaptic inhibition of Ia EPSPs in cat spinal motoneurones. J Physiol 447:675-692. Medline
57. Tergau F, Wanschura V, Canelo M, Wischer S, Wassermann EM, Ziemann U, Paulus W (1999) Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation. Exp Brain Res 124:447-454. CrossRef Medline
58. Thomas CK, Häger-Ross CK, Klein CS (2010) Effects of baclofen on motor units paralysed by chronic cervical spinal cord injury. Brain 133:117-125. CrossRef Medline
59. Tillakaratne NJ, Mouria M, Ziv NB, Roy RR, Edgerton VR, Tobin AJ (2000) Increased expression of glutamate decarboxylase (GAD(67) in feline lumbar spinal cord after complete thoracic spinal cord transection. J Neurosci Res 60:219-230. CrossRef Medline
60. Tillakaratne NJ, de Leon RD, Hoang TX, Roy RR, Edgerton VR, Tobin AJ (2002) Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J Neurosci 22:3130-3143. Medline
61. Valls-Solé J, Pascual-Leone A, Wassermann EM, Hallett M (1992) Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 85:355-364. Medline
62. Wallace DM, Ross BH, Thomas CK (2012) Characteristics of lower extremity clonus after human cervical spinal cord injury. J Neurotrauma 29:915-924. CrossRef Medline
63. Wassermann EM, Samii A, Mercuri B, Ikoma K, Oddo D, Grill SE, Hallett M (1996) Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles. Exp Brain Res 109: 158-163. Medline
64. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517:591-597. CrossRef Medline
65. Willerslev-Olsen M, Lundbye-Jensen J, Petersen TH, Nielsen JB (2011) The effect of baclofen and diazepam on motor skill acquisition in healthy subjects. Exp Brain Res 213:465-474. CrossRef Medline
66. Yang K, Wang D, Li YQ (2001) Distribution and depression of the GABAB receptor in the spinal dorsal horn of adult rat. Brain Res Bull 55:479-485. CrossRef Medline
67. Ziemann U, Lönnecker S, Steinhoff BJ, PaulusW (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367-378. CrossRef Medline