Cortical control of adaptive locomotion in wild-type mice and mutant mice lacking the ephrin-Eph effector protein α2-chimaerin

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3189-3202

  Asante, Curtis Oware ^a,b   Chu, Amy ^a   Fisher, Mark ^a   Benson, Leora ^a   Beg, Asim ^a,c   Scheiffele, Peter ^a,d   Martin, John ^a,b,e  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF BASEL   (Switzerland)

^e NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIN; EPHRIN A4; EPHRIN B3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FORELIMB; INTERNEURON; LOCOMOTION; MALE; MOTOR CORTEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; VOLUNTARY MOVEMENT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AXONAL TRANSPORT; BIOMECHANICS; CHIMERIN 1; EPHRIN-A4; EPHRIN-B3; FEMALE; FORELIMB; GAIT DISORDERS, NEUROLOGIC; HERPESVIRUS 1, SUID; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MOTOR CORTEX; PROTEIN ISOFORMS; PYRAMIDAL TRACTS; RUNNING; SPINAL CORD;

EID: 78650867531     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00671.2010     Document Type: Article

References (49)

1. Akay T, Acharya HJ, Fouad K, Pearson KG. Behavioral and electromyographic characterization of mice lacking EphA4 receptors. J Neurophysiol 96: 642-651, 2006.
2. Armstrong DM. The supraspinal control of mammalian locomotion. J Physiol 405: 1-37, 1988.
3. Banfield BW, Kaufman JD, Randall JA, Pickard GE. Development of pseudorabies virus strains expressing red fluorescent proteins: New tools for multisynaptic labeling applications. J Virol 77: 10106-10112, 2003.
4. Bareyre FM, Kerschensteiner M, Misgeld T, Sanes JR. Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat Med 11: 1355-1360, 2005.
5. Beg AA, Sommer JE, Martin JH, Scheiffele P. alpha2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 55: 768-778, 2007.
6. Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, Parada LF. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci USA 102: 10694-10699, 2005.
7. Brouwer B, Ashby P. Altered corticospinal projections to lower limb motoneurons in subjects with cerebral palsy. Brain 114: 1395-1407, 1991.
8. Brown TG. On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J Physiol 48: 1-17, 1914.
9. Brus-Ramer M, Carmel JB, Martin JH. Motor cortex bilateral motor representation depends on subcortical and interhemispheric interactions. J Neurosci 29: 6196-6206, 2009.
10. Carr LJ, Harrison LM, Evans AL, Stephens JA. Patterns of central motor reorganization in hemiplegic cerebral palsy. Brain 116: 1223-1247, 1993.
11. Cheney PD, Fetz EE, Mewes K. Neural mechanisms underlying coricospinal and rubrospinal control of limb movements. Prog Brain Res 87: 213-252, 1991.
12. Coonan JR, Greferath U, Messenger J, Hartley L, Murphy M, Boyd AW, Dottori M, Galea MP, Bartlett PF. Development and reorganization of corticospinal projections in EphA4 deficient mice. J Comp Neurol 436: 248-262, 2001.
13. Drew T. Motor cortical discharge during voluntary gait modification. Brain Res 457: 181-187, 1988.
14. Drew T, Andujar JE, Lajoie K, Yakovenko S. Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res Rev 57: 199-211, 2008.
15. Drew T, Prentice S, Schepens B. Cortical and brainstem control of locomotion. Prog Brain Res 143: 251-261, 2004.
16. Eyre JA, Smith M, Dabydeen L, Clowry GJ, Patacchi E, Battini R, Guzzetta A, Cioni G. Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system? Ann Neurol 62: 493-503, 2007.
17. Fanardjian VV, Papoyan EV. Patterns of inputs to the parietal cortex efferent neurons from the motor cortex and cerebellum in the cat. Neuroscience 77: 965-974, 1997.
18. Farmer SF, Harrison LM, Ingram DA, Stephens JA. Plasticity of central motor pathways in children with hemiplegic cerebral palsy. Neurology 41: 1505-1510, 1991.
19. Friel K, Martin JH. Bilateral activity-dependent interactions in the developing corticospinal system. J Neurosci 27: 11083-11090, 2007. (Pubitemid 47574163)
20. Friel KM, Drew T, Martin JH. Differential activity-dependent development of corticospinal control of movement and final limb position during visuallyguided locomotion. J Neurophysiol 97: 3396-3406, 2007.
21. Georgopoulos AP. On reaching. Annu Rev Neurosci 9: 147-170, 1986.
22. Georgopoulos AP, Grillner S. Visuomotor coordination in reaching and locomotion. Science 245: 1209-1210, 1989.
23. Goulding M. Circuits controlling vertebrate locomotion: Moving in a new direction. Nat Rev Neurosci 10: 507-518, 2009.
24. Iwasato T, Katoh H, Nishimaru H, Ishikawa Y, Inoue H, Saito YM, Ando R, Iwama M, Takahashi R, Negishi M, Itohara S. Rac-GAP alphachimerin regulates motor-circuit formation as a key mediator of ephrinB3/ ephA4 forward signaling. Cell 130: 742-753, 2007.
25. Jiang W, Drew T. Effects of bilateral lesions of the dorsolateral funiculi and dorsal columns at the level of the low thoracic spinal cord on the control of locomotion in the adult cat. I. Treadmill walking. J Neurophysiol 76: 849-866, 1996.
26. 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, 2009.
27. Krouchev N, Kalaska JF, Drew T. Sequential activation of muscle synergies during locomotion in the intact cat as revealed by cluster analysis and direct decomposition. J Neurophysiol 96: 1991-2010, 2006.
28. Kullander K, Butt SJ, Lebret JM, Lundfald L, Restrepo CE, Rydstrom A, Klein R, Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299: 1889-1892, 2003.
29. Kullander K, Croll SD, Zimmer M, Pan L, McClain J, Hughes V, Zabski S, DeChiara TM, Klein R, Yancopoulos GD, Gale NW. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev 15: 877-888, 2001.
30. Kuypers HGJM. Anatomy of the descending pathways. In: Handbook of Physiology, Neurophysiology, edited by Brookhart JM, Mountcastle VB. Bethesda, MD: American Physiological Society, 1981, vol. 2, p. 597-666.
31. Lavoie S, Drew T. Discharge characteristics of neurons in the red nucleus during voluntary gait modifications: A comparison with the motor cortex. J Neurophysiol 88: 1791-1814, 2002.
32. Li C-X, Waters RS. Organization of the mouse motor cortex studied by retrograde tracing and intracortical microstimulation (ICMS) mapping. Can J Neurol Sci 18: 28-38, 1991.
33. Martin JH, Ghez C. Red nucleus and motor cortex: Parallel motor systems for the initiation and control of skilled movement. Behav Brain Res 28: 217-223, 1988.
34. Mayston MJ, Harrison LM, Quinton R, Stephens JA, Krams M, Bouloux PM. Mirror movements in X-linked Kallmann's syndrome. I. A neurophysiological study. Brain 120: 1199-1216, 1997. (Pubitemid 27285737)
35. McKenna JE, Prusky GT, Whishaw IQ. Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: A retrograde carbocyanine dye analysis. J Comp Neurol 419: 286-296, 2000.
36. McVea DA, Pearson KG. Stepping of the forelegs over obstacles establishes long-lasting memories in cats. Curr Biol 17: R621-R-623, 2007.
37. Muller K, Kass-Iliyya F, Reitz M. Ontogeny of ipsilateral corticospinal projections: A developmental study with transcranial magnetic stimulation. Ann Neurol 42: 705-711, 1997.
38. Patla AE, Rietdyk S, Martin C, Prentice S. Locomotor patterns of the leading and the trailing limbs as solid and fragile obstacles are stepped over: Some insights into the role of vision during locomotion. J Motor Behav 28: 35-47, 1996.
39. Pearson K, Gramlich R. Updating neural representations of objects during walking. Ann NY Acad Sci 1198: 1-9, 2010.
40. Rathelot JA, Strick PL. Muscle representation in the macaque motor cortex: An anatomical perspective. Proc Natl Acad Sci USA 103: 8257-8262, 2006.
41. Rathelot JA, Strick PL. Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci USA 106: 918-923, 2009.
42. Rho MJ, Cabana T, Drew T. Organization of the projections from the pericruciate cortex to the pontomedullary reticular formation of the cat: A quantitative retrograde tracing study. J Comp Neurol 388: 228-249, 1997.
43. Salimi I, Friel K, Martin JH. Pyramidal tract stimulation restores normal corticospinal tract connections and visuomotor skill after early postnatal motor cortex activity blockade. J Neurosci 28: 7426-7434, 2008.
44. Shi L, Fu WY, Hung KW, Porchetta C, Hall C, Fu AK, Ip NY. Alpha2- chimaerin interacts with EphA4 and regulates EphA4-dependent growth cone collapse. Proc Natl Acad Sci USA 104: 16347-16352, 2007.
45. Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, Pickard GE. Pseudorabies virus expressing enhanced green fluorescent protein: A tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci USA 97: 9264-9269, 2000.
46. Srour M, Riviere JB, Pham JM, Dube MP, Girard S, Morin S, Dion PA, Asselin G, Rochefort D, Hince P, Diab S, Sharafaddinzadeh N, Chouinard S, Theoret H, Charron F, Rouleau GA. Mutations in DCC cause congenital mirror movements. Science 328: 592, 2010.
47. Vulliemoz S, Raineteau O, Jabaudon D. Reaching beyond the midline: Why are human brains cross wired? Lancet Neurol 4: 87-99, 2005.
48. Wegmeyer H, Egea J, Rabe N, Gezelius H, Filosa A, Enjin A, Varoqueaux F, Deininger K, Schnutgen F, Brose N, Klein R, Kullander K, Betz A. EphA4-dependent axon guidance is mediated by the RacGAP alpha2- chimaerin. Neuron 55: 756-767, 2007.
49. Z'Graggen WJ, Fouad K, Raineteau O, Metz GA, Schwab ME, Kartje GI. Compensatory sprouting and impulse rerouting after unilateral pyramidal tract lesion in neonatal rats. J Neurosci 20: 6561-6569, 2000.