Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey

Brain

Volumn 135, Issue 7, 2012, Pages 2277-2289

  Zaaimi, Boubker ^a   Edgley, Steve A ^b   Soteropoulos, Demetris S ^a   Baker, Stuart N ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Plasticity; Post stroke recovery; Primate; Pyramidal tract lesion; Reticulospinal tract

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLIMBING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; FINGER; FLACCID PARALYSIS; MACACA; MEDIAL LONGITUDINAL FASCICULUS; MOTONEURON; MOTOR PERFORMANCE; MUSCLE INNERVATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL SIGN; PYRAMIDAL TRACT;

EID: 84863216165     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws115     Document Type: Article

References (52)

1. Alstermark B, Isa T, Ohki Y, Saito Y. Disynaptic pyramidal excitation in forelimb motoneurons mediated via C(3)-C(4) propriospinal neurons in the Macaca fuscata. J Neurophysiol 1999; 82: 3580-5. (Pubitemid 30017477)
2. Baker SN. The primate reticulospinal tract, hand function and functional recovery. J Physiol 2011; 589: 5603-12.
3. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 2004; 7: 269-77. (Pubitemid 38280451)
4. Belhaj-Saif A, Cheney PD. Plasticity in the distribution of the red nucleus output to forearm muscles after unilateral lesions of the pyramidal tract. J Neurophysiol 2000; 83: 3147-53. (Pubitemid 30321502)
5. Benecke R, Meyer BU, Freund HJ. Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation. Exp Brain Res 1991; 83: 419-26.
6. Calautti C, Leroy F, Guincestre JY, Marie RM, Baron JC. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport 2001; 12: 3883-6. (Pubitemid 33152417)
7. Cauraugh J, Light K, Kim S, Thigpen M, Behrman A. Chronic motor dysfunction after stroke: recovering wrist and finger extension by electromyography-triggered neuromuscular stimulation. Stroke 2000; 31: 1360-4. (Pubitemid 30351258)
8. Chapman CE, Wiesendanger M. Recovery of function following unilateral lesions of the bulbar pyramid in the monkey. Electroencephalogr Clin Neurophysiol 1982; 53: 374-87. (Pubitemid 12150630)
9. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997; 28: 2518-27. (Pubitemid 28007661)
10. Davidson AG, Buford JA. Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging. Exp Brain Res 2006; 173: 25-39. (Pubitemid 44099697)
11. Davidson AG, Schieber MH, Buford JA. Bilateral spike-triggered average effects in arm and shoulder muscles from the monkey pontomedullary reticular formation. J Neurosci 2007; 27: 8053-8. (Pubitemid 47173304)
12. Dewald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ. Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain 1995; 118: 495-510.
13. Edgley SA, Jankowska E, Krutki P, Hammar I. Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents. J Physiol 2003; 552: 961-74. (Pubitemid 37428434)
14. Fritz SL, Light KE, Patterson TS, Behrman AL, Davis SB. Active finger extension predicts outcomes after constraint-induced movement therapy for individuals with hemiparesis after stroke. Stroke; a journal of cerebral circulation 2005; 36: 1172-7. (Pubitemid 40798734)
15. Hepp-Reymond MC, Wiesendanger M. Unilateral pyramidotomy in monkeys: Effects on force and speed of a conditioned precision grip. Brain Res 1972; 36: 117-31.
16. Hepp-Reymond MC, Trouche E, Wiesendanger M. Effects of unilateral and bilateral pyramidotomy on a conditioned rapid precision grip in monkeys (macaca fascicularis). Exp Brain Res 1974; 21: 519-27.
17. Illert M, Jankowska E, Lundberg A, Odutola A. Integration in descending motor pathways controlling the forelimb in the cat. 7. Effects from the reticular formation on C3-C4 propriospinal neurones. Exp Brain Res 1981; 42: 269-81. (Pubitemid 11112358)
18. Kuypers HGJM. Anatomy of the descending pathways. In: Brookhart JM, Mountcastle VB, editors. Handbook of Physiology - The Nervous System II. Bethesda, MD: American Physiological Society; 1981. p. 597-666.
19. Lawrence DG, Kuypers HGJM. The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathway. Brain 1968a; 91: 15-36.
20. Lawrence DG, Kuypers HGJM. The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 1968b; 91: 1-14.
21. Lemon RN. Cortical control of the primate hand. The 1992 G.L. Brown Prize Lecture. Exp Physiol 1993; 78: 263-301.
22. Maier MA, Illert M, Kirkwood PA, Nielsen J, Lemon RN. Does a C3-C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey. J Physiol 1998; 511: 191-212. (Pubitemid 28421323)
23. Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 2000; 31: 656-61. (Pubitemid 30131651)
24. Martin RF, Bowden DM. A stereotaxic template atlas of the macaque brain for digital imaging and quantitative neuroanatomy. Neuroimage 1996; 4: 119-50. (Pubitemid 26337405)
25. Matsuyama K, Takakusaki K, Nakajima K, Mori S. Multi-segmental innervation of single pontine reticulospinal axons in the cervico-thoracic region of the cat: anterograde PHA-L tracing study. J Comp Neurol 1997; 377: 234-50. (Pubitemid 27009831)
26. Matsuyama K, Mori F, Kuze B, Mori S. Morphology of single pontine reticulospinal axons in the lumbar enlargement of the cat: a study using the anterograde tracer PHA-L. J Comp Neurol 1999; 410: 413-30. (Pubitemid 29296201)
27. Mazevet D, Meunier S, Pradat-Diehl P, Marchand-Pauvert V, Pierrot- Deseilligny E. Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. Brain 2003; 126: 988-1000. (Pubitemid 36372995)
28. Mewes K, Cheney PD. Facilitation and suppression of wrist and digit muscles from single rubromotoneuronal cells in the awake monkey. J Neurophysiol 1991; 66: 1965-77.
29. Morecraft RJ, McNeal DW, Stilwell-Morecraft KS, Dvanajscak Z, Ge J, Schneider P. Localization of arm representation in the cerebral peduncle of the non-human primate. J Comp Neurol 2007; 504: 149-67. (Pubitemid 47327475)
30. Nathan PW, Smith MC. Long descending tracts in man. I. Review of present knowledge. Brain 1955; 78: 248-303.
31. Netz J, Lammers T, Homberg V. Reorganization of motor output in the non-affected hemisphere after stroke. Brain 1997; 120: 1579-86. (Pubitemid 27389225)
32. Nielsen J, Pierrot-Deseilligny E. Pattern of cutaneous inhibition of the propriospinal-like excitation to human upper limb motoneurones. J Physiol 1991; 434: 169-82.
33. Nishimura Y, Onoe H, Morichika Y, Perfiliev S, Tsukada H, Isa T. Time-dependent central compensatory mechanisms of finger dexterity after spinal cord injury. Science 2007; 318: 1150-5. (Pubitemid 350134900)
34. Nishimura Y, Isa T. Compensatory changes at the cerebral cortical level after spinal cord injury. Neuroscientist 2009; 15: 436-44.
35. Olivier E, Baker SN, Nakajima K, Brochier T, Lemon RN. Investigation into non-monosynaptic corticospinal excitation of macaque upper limb single motor units. J Neurophysiol 2001; 86: 1573-86. (Pubitemid 32953209)
36. Onodera S, Hicks TP. Carbocyanine dye usage in demarcating boundaries of the aged human red nucleus. PloS one 2010; 5: e14430.
37. Peterson BW, Maunz RA, Pitts NG, Mackel RG. Patterns of projection and braching of reticulospinal neurons. Exp Brain Res 1975; 23: 333-51.
38. Porter R. Early facilitation at corticomotoneuronal synapses. J Physiol 1970; 207: 733-45.
39. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. Numerical recipies in Pascal. Cambridge: Cambridge University Press; 1989.
40. Rathelot J-A, Strick PL. Muscle representation in the macaque motor cortex: An anatomical perspective. PNAS 2006; 103: 8257-62. (Pubitemid 43801085)
41. Riddle CN, Edgley SA, Baker SN. Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 2009; 29: 4993-9.
42. Rosenzweig ES, Brock JH, Culbertson MD, Lu P, Moseanko R, Edgerton VR, et al. Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys. J Comp Neurol 2009; 513: 151-63.
43. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 2010; 13: 1505-10.
44. Sasaki S, Isa T, Pettersson LG, Alstermark B, Naito K, Yoshimura K, et al. Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. J Neurophysiol 2004; 92: 3142-7. (Pubitemid 40340519)
45. Schepens B, Drew T. Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. J Neurophysiol 2006; 96: 2229-52. (Pubitemid 44785879)
46. Schwartzman RJ. A behavioral analysis of complete unilateral section of the pyramidal tract at the medullary level in Macaca mulatta. Ann Neurol 1978; 4: 234-44. (Pubitemid 8389818)
47. Soteropoulos DS, Edgley SA, Baker SN. Lack of evidence for direct corticospinal contributions to control of the ipsilateral forelimb in monkey. J Neurosci 2011; 31: 11208-19.
48. Tower SS. Pyramidal lesion in the monkey. Brain 1940; 63: 36-90.
49. Twitchell TE. The restoration of motor fucntion following hemiplegia in man. Brain 1951; 74: 443-80.
50. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 2003a; 126: 2476-96. (Pubitemid 37314437)
51. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain 2003b; 126: 1430-48. (Pubitemid 36644387)
52. Yoshino-Saito K, Nishimura Y, Oishi T, Isa T. Quantitative intersegmental and inter-laminar comparison of corticospinal projections from the forelimb area of the primary motor cortex of macaque monkeys. Neuroscience 2010; 171: 1164-79.