Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries

Journal of Neuroscience

Volumn 31, Issue 25, 2011, Pages 9264-9278

  Musienko, Pavel ^a,b   van den Brand, Rubia ^a   Märzendorfer, Olivia ^a,c   Roy, Roland R ^d   Gerasimenko, Yury ^b,d   Edgerton, V Reggie ^d,e   Courtine, Grégoire ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; DOPAMINE RECEPTOR; SEROTONIN RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMECHANICS; BODY EQUILIBRIUM; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; LOCOMOTION; MONOAMINERGIC SYSTEM; MOTOR COORDINATION; NEUROMODULATION; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SPINAL CORD; SPINAL CORD STIMULATION; STATISTICAL ANALYSIS; WEIGHT BEARING;

ANIMALS; BEHAVIOR, ANIMAL; BIOGENIC MONOAMINES; FEMALE; GAIT; LOCOMOTION; NERVE NET; NEURAL PATHWAYS; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 79959680662     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5796-10.2011     Document Type: Article

References (41)

1. Agnati LF, Fuxe K (2000) Volume transmission as a key feature of information handling in the central nervous system possible new interpretative value of the Turing's B-type machine. Prog Brain Res 125:3-19.
2. Agnati LF, Guidolin D, Guescini M, Genedani S, Fuxe K (2010) Understanding wiring and volume transmission. Brain Res Rev 64:137-159.
3. Antri M, Mouffle C, Orsal D, Barthe JY (2003) 5-HT1A receptors are involved in short- and long-term processes responsible for 5-HT-induced locomotor function recovery in chronic spinal rat. Eur J Neurosci 18:1963-1972.
4. Barbeau H, Rossignol S (1991) Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res 546:250-260.
5. Carhart MR, He J, Herman R, D'Luzansky S, Willis WT (2004) Epidural spinal-cord stimulation facilitates recovery of functional walking following incomplete spinal-cord injury. IEEE Trans Neural Syst Rehabil Eng 12:32-42.
6. Chau C, Barbeau H, Rossignol S (1998a) Early locomotor training with clonidine in spinal cats. J Neurophysiol 79:392-409.
7. Chau C, Barbeau H, Rossignol S (1998b) Effects of intrathecal alpha1- and alpha2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J Neurophysiol 79:2941-2963.
8. Courtine G, Roy RR, Raven J, Hodgson J, McKay H, Yang H, Zhong H, Tuszynski MH, Edgerton VR (2005) Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta). Brain 128:2338-2358.
9. Courtine G, Song B, Roy RR, Zhong H, Herrmann JE, Ao Y, Qi J, Edgerton VR, Sofroniew MV (2008) Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 14:69-74.
10. 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 (2009) Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12:1333-1342.
11. Delivet-Mongrain H, Leblond H, Rossignol S (2008) Effects of localized intraspinal injections of a noradrenergic blocker on locomotion of high decerebrate cats. J Neurophysiol 100:907-921.
12. Dietz V, Colombo G, Jensen L, Baumgartner L (1995) Locomotor capacity of spinal cord in paraplegic patients. Ann Neurol 37:574-582.
13. Fong AJ, Roy RR, Ichiyama RM, Lavrov I, Courtine G, Gerasimenko Y, Tai YC, Burdick J, Edgerton VR (2009) Recovery of control of posture and locomotion after a spinal cord injury: solutions staring us in the face. Prog Brain Res 175:393-418.
14. Gerasimenko YP, Ichiyama RM, Lavrov IA, Courtine G, Cai L, Zhong H, Roy RR, Edgerton VR (2007) Epidural spinal cord stimulation plus quipazine administration enable stepping in complete spinal adult rats. J Neurophysiol 98:2525-2536.
15. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751-766.
16. Grillner S, Zangger P (1979) On the central generation of locomotion in the low spinal cat. Exp Brain Res 34:241-261.
17. Guertin PA (2009) Recovery of locomotor function with combinatory drug treatments designed to synergistically activate specific neuronal networks. Curr Med Chem 16:1366-1371.
18. Guertin PA, Steuer I (2005) Ionotropic 5-HT3 receptor agonist-inducedmotor responses in the hindlimbs of paraplegic mice. J Neurophysiol 94:3397-3405.
19. Guertin PA, Ung RV, Rouleau P, Steuer I (2011) Effects on locomotion, muscle, bone, and blood induced by a combination therapy eliciting weight-bearing stepping in nonassisted spinal cord-transected mice. Neurorehabil Neural Repair 25:234-242.
20. Hägglund M, Borgius L, Dougherty KJ, Kiehn O (2010) Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 13:246-252.
21. Han P, Nakanishi ST, Tran MA, Whelan PJ (2007) Dopaminergic modulation of spinal neuronal excitability. J Neurosci 27:13192-13204.
22. Harkema SJ, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y, Ferreira CK, Rejc E, Edgerton VR (2010) Sensory control of standing and steppingenabled by epidural stimulation after a human motor complete spinal cord injury. Soc Neurosci Abstr 36:259-251.
23. Hochman S, Garraway S, Machacek D, Shay B (2001) 5-HT receptors and the neuromodulatory control of spinal cord function. In: Motor neurobiology of the spinal cord (Raton B, ed), pp 47-87. Boca Raton, FL: CRC.
24. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG (2008) Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57:183-191.
25. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
26. Landry ES, Lapointe NP, Rouillard C, Levesque D, Hedlund PB, Guertin PA (2006) Contribution of spinal 5-HT1A and 5-HT7 receptors to locomotor-like movement induced by 8-OH-DPAT in spinal cordtransected mice. Eur J Neurosci 24:535-546.
27. Lapointe NP, Guertin PA (2008) Synergistic effects of D1/5 and 5-HT1A/7 receptor agonists on locomotor movement induction in complete spinal cord-transected mice. J Neurophysiol 100:160-168.
28. Lapointe NP, Rouleau P, Ung RV, Guertin PA (2009) Specific role of D1 receptors in spinal network activation and rhythmic movement induction in vertebrates. J Physiol 587:1499-1511.
29. Lavrov I, Gerasimenko YP, Ichiyama RM, Courtine G, Zhong H, Roy RR, Edgerton VR (2006) Plasticity of spinal cord reflexes after a complete transection in adult rats: relationship to stepping ability. J Neurophysiol 96:1699-1710.
30. Lavrov I, Dy CJ, Fong AJ, Gerasimenko Y, Courtine G, Zhong H, Roy RR, Edgerton VR (2008) Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J Neurosci 28:6022-6029.
31. Liu J, Jordan LM (2005) Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J Neurophysiol 94:1392-1404.
32. Liu J, Akay T, Hedlund PB, Pearson KG, Jordan LM (2009) Spinal 5-HT7 receptors are critical for alternating activity during locomotion: in vitroneonatal and in vivo adult studies using 5-HT7 receptor knockout mice. J Neurophysiol 102:337-348.
33. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ (2004) Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92: 1566-1576.
34. Morales M, Battenberg E, Bloom FE (1998) Distribution of neurons expressing immunoreactivity for the 5HT3 receptor subtype in the rat brain and spinal cord. J Comp Neurol 402:385-401.
35. Musienko P, van den Brand R, Maerzendorfer O, Larmagnac A, Courtine G (2009) Combinatory electrical and pharmacological neuroprosthetic interfaces to regain motor function after spinal cord injury. IEEE Trans Biomed Eng 56:2707-2711.
36. Noga BR, Johnson DM, Riesgo MI, Pinzon A (2009) Locomotor-activated neurons of the cat. I. Serotonergic innervation and co-localization of 5-HT7, 5-HT2A, and 5-HT1A receptors in the thoraco-lumbar spinal cord. J Neurophysiol 102:1560-1576.
37. Okado N, Homma S, Ishihara R, Sako H, Kohno K (1988) Differential innervation of specific motor neuron pools by serotoninergic fibers in the chick spinal cord. Neurosci Lett 94:29-32.
38. Raymond JR, Mukhin YV, Gelasco A, Turner J, Collinsworth G, Gettys TW, Grewal JS, Garnovskaya MN (2001) Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol Ther 92: 179-212.
39. Riddell JS, Jankowska E, Eide E (1993) Depolarization of group II muscle afferents by stimuli applied in the locus coeruleus and raphe nuclei of the cat. J Physiol 461:723-741.
40. Wachtel SR, White FJ (1995) The dopamine D1 recepto r antagonist SCH 23390 can exertD1 agonist-like effects on rat nucleus accumbens neurons. Neurosci Lett 199:13-16.
41. Zoli M, Jansson A, Syková E, Agnati LF, Fuxe K (1999) Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol Sci 20:142-150.