Sprouting of brainstem-spinal tracts in response to unilateral motor cortex stroke in mice

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3378-3389

  Bachmann, Lukas C ^a,b   Lindau, Nicolas T ^a,b   Felder, Petra ^a,b   Schwab, Martin E ^a,b  

^a University of Zurich Brain Research Institute   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

Brainstem; Plasticity; Recovery; Sprouting; Stroke; Tracing

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTEROGRADE TRACING; ARTICLE; BRAIN STEM; CEREBROVASCULAR ACCIDENT; CLIMBING; CONTROLLED STUDY; CYLINDER TEST; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; GRID WALKING TEST; INVESTIGATIVE PROCEDURES; LATERAL VESTIBULAR NUCLEUS; LOCOMOTION; MOTOR CORTEX; MOUSE; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; RAPHE NUCLEUS; RETROGRADE MUSCLE TRACING; RETROGRADE TRACING; ROTAROD TEST; TASK PERFORMANCE; TRIGEMINAL NUCLEUS; VERTICAL ROPE TEST;

BRAINSTEM; PLASTICITY; RECOVERY; SPROUTING; STROKE; TRACING;

ANIMALS; BIOTIN; BRAIN STEM; DEXTRANS; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENT DYES; FUNCTIONAL LATERALITY; LOCOMOTION; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; MOTOR CORTEX; MUSCLE STRENGTH; NEURAL PATHWAYS; PSYCHOMOTOR PERFORMANCE; ROTAROD PERFORMANCE TEST; SPINAL CORD; STROKE; TIME FACTORS;

EID: 84894418175     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4384-13.2014     Document Type: Article

References (54)

1. Bach LM, MagounHW (1947) The vestibular nuclei as an excitatory mechanism for the cord. J Neurophysiol 10:331-337. Medline
2. Bácskai T, Fu Y, Sengul G, Rusznák Z, Paxinos G, Watson C (2013) Musculotopic organization of the motor neurons supplying forelimb and shoulder girdle muscles in the mouse. Brain Struct Funct 218:221-238. CrossRef Medline
3. Baker SN (2011) The primate reticulospinal tract, hand function and functional recovery. J Physiol 589:5603-5612. CrossRef Medline
4. Benecke R, Meyer BU, Freund HJ (1991) Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation. Exp Brain Res 83: 419-426. Medline
5. Berridge KC (1989) Progressive degradation of serial grooming chains by descending decerebration. Behav Brain Res 33:241-253. CrossRef Medline
6. Bignall KE, Schramm L (1974) Behavior of chronically decerebrated kittens. Exp Neurol 42:519-531. CrossRef Medline
7. Bowker RM, Westlund KN, Coulter JD (1981) Origins of serotonergic projections to the spinal cord in rat: an immunocytochemical-retrograde transport study. Brain Res 226:187-199. CrossRef Medline
8. Brus-Ramer M, Carmel JB, Chakrabarty S, Martin JH (2007) Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. J Neurosci 27:13793-13801. CrossRef Medline
9. Bury SD, Jones TA (2002) Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the "unaffected" forelimb and training-induced dendritic structural plasticity in the motor cortex. J Neurosci 22:8597-8606. Medline
10. Caramia MD, Iani C, Bernardi G (1996) Cerebral plasticity after stroke as revealed by ipsilateral responses to magnetic stimulation. Neuroreport 7:1756-1760. CrossRef Medline
11. Cheng H, Olson L (1995) A new surgical technique that allows proximodistal regeneration of 5-HT fibers after complete transection of the rat spinal cord. Exp Neurol 136:149-161. CrossRef Medline
12. Gamper E (1926) Bau und Leistungen eines menschlichen Mittelhirnwesens (Arhinencephalie mit Encephalocele) zugleich ein Beitrag zur Teratologie und Fasersystematik. Zeitschrift Neurologie Psychiatrie 102: 154-235. CrossRef
13. Ghosh A, Sydekum E, Haiss F, Peduzzi S, Zörner B, Schneider R, Baltes C, Rudin M, Weber B, Schwab ME (2009) Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J Neurosci 29:12210-12219. CrossRef Medline
14. Hallett M (2001) Functional reorganization after lesions of the human brain: studies with transcranial magnetic stimulation. Rev Neurol (Paris) 157:822-826. CrossRef Medline
15. Heffner RS, Masterton RB (1983) The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav Evol 23:165-183. CrossRef Medline
16. Herzog A, Brösamle C (1997) 'Semifree-floating' treatment: a simple and fast method to process consecutive sections for immunohistochemistry and neuronal tracing. J Neurosci Methods 72:57-63. CrossRef Medline
17. Isa T, Ohki Y, Alstermark B, Pettersson LG, Sasaki S (2007) Direct and indirect cortico-motoneuronal pathways and control of hand/arm movements. Physiology 22:145-152. CrossRef Medline
18. Jankowska E, Edgley SA (2006) How can corticospinal tract neurons contribute to ipsilateral movements? A question with implications for recovery of motor functions. Neuroscientist 12:67-79. CrossRef Medline
19. Kartje-Tillotson G, Neafsey EJ, Castro AJ (1985) Electrophysiological analysis of motor cortical plasticity after cortical lesions in newborn rats. Brain Res 332:103-111. CrossRef Medline
20. Kennedy PR (1990) Corticospinal, rubrospinal and rubro-olivary projections: a unifying hypothesis. Trends Neurosci 13:474-479. CrossRef Medline
21. Lawrence DG, Kuypers HG (1968a) The functional organization of the motor system in the monkey: I. The effects of bilateral pyramidal lesions. Brain 91:1-14. CrossRef Medline
22. Lawrence DG, KuypersHG (1968b) The functional organization of the motor system in the monkey: II. The effects of lesions of the descending brain-stem pathways. Brain 91:15-36. CrossRef Medline
23. Lee JK, Park MS, Kim YS, Moon KS, Joo SP, Kim TS, Kim JH, Kim SH (2007) Photochemically induced cerebral ischemia in a mouse model. Surg Neurol 67:620-625, discussion 625. CrossRef Medline
24. Liang H, Paxinos G, Watson C (2011) Projections from the brain to the spinal cord in the mouse. Brain Struct Funct 215:159-186. CrossRef Medline
25. Liang H, Paxinos G, WatsonC (2012) Spinal projections from the presumptive midbrain locomotor region in the mouse. Brain Struct Funct 217: 211-219. CrossRef Medline
26. Liu Z, Chopp M, Ding X, Cui Y, Li Y (2013) Axonal remodeling of the corticospinal tract in the spinal cord contributes to voluntary motor recovery after stroke in adult mice. Stroke 44:1951-1956. CrossRef Medline
27. Maier IC, Baumann K, Thallmair M, Weinmann O, Scholl J, Schwab ME (2008) Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury. J Neurosci 28:9386-9403. CrossRef Medline
28. McKenna JE, Prusky GT, Whishaw IQ (2000) 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. CrossRef Medline
29. Nakagawa H, Ueno M, Itokazu T, Yamashita T (2013) Bilateral movement training promotes axonal remodeling of the corticospinal tract and recovery of motor function following traumatic brain injury in mice. Cell Death Dis 4:e534. CrossRef Medline
30. Nudo RJ, Wise BM, SiFuentes F, Milliken GW (1996) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272:1791-1794. CrossRef Medline
31. Nygren LG, Fuxe K, Jonsson G, Olson L (1974) Functional regeneration of 5-hydroxytryptamine nerve terminals in the rat spinal cord following 5,6-dihydroxytryptamine induced degeneration. Brain Res 78:377-394. CrossRef Medline
32. Omoto S, Ueno M, Mochio S, Yamashita T (2011) Corticospinal tract fibers cross the ephrin-B3-negative part of the midline of the spinal cord after brain injury. Neurosci Res 69:187-195. CrossRef Medline
33. Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263-273. CrossRef Medline
34. Riddle CN, Baker SN (2010) Convergence of pyramidal and medial brain stem descending pathways onto macaque cervical spinal interneurons. J Neurophysiol 103:2821-2832. CrossRef Medline
35. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, Nout YS, Roy RR, Miller DM, Beattie MS, Havton LA, Bresnahan JC, Edgerton VR, TuszynskiMH (2010) Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13:1505-1510. CrossRef Medline
36. Rossini PM, Calautti C, Pauri F, Baron JC (2003) Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2:493-502. CrossRef Medline
37. Rouiller EM, Liang FY, Moret V, Wiesendanger M (1991) Trajectory of redirected corticospinal axons after unilateral lesion of the sensorimotor cortex in neonatal rat: a phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Exp Neurol 114:53-65. CrossRef Medline
38. Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M (1994) Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res 102:227-243. CrossRef Medline
39. Schmidt BJ, Jordan LM (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53:689-710. CrossRef Medline
40. Shanina EV, Schallert T, Witte OW, Redecker C (2006) Behavioral recovery from unilateral photothrombotic infarcts of the forelimb sensorimotor cortex in rats: role of the contralateral cortex. Neuroscience 139:1495-1506. CrossRef Medline
41. Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, RossiniPM (2002) Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 125:1896-1907. CrossRef Medline
42. Soteropoulos DS, Williams ER, Baker SN (2012) Cells in the monkey pontomedullary reticular formation modulate their activity with slow finger movements. J Physiol 590:4011-4027. CrossRef Medline
43. Starkey ML, Bleul C, Zörner B, Lindau NT, Mueggler T, Rudin M, Schwab ME (2012) Back seat driving: hindlimb corticospinal neurons assume forelimb control following ischaemic stroke. Brain 135:3265-3281. CrossRef Medline
44. Taub E, Crago JE, Burgio LD, Groomes TE, CookEW3rd, DeLuca SC, Miller NE (1994) An operant approach to rehabilitation medicine: overcoming learned nonuse by shaping. J Exp Anal Behav 61:281-293. CrossRef Medline
45. Tennant KA, Adkins DL, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA (2011) The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb Cortex 21:865-876. CrossRef Medline
46. Travis AM, Woolsey CN (1956) Motor performance of monkeys after bilateral partial and total cerebral decortications. Am J Phys Med 35:273-310. Medline
47. Ueno M, Hayano Y, Nakagawa H, Yamashita T (2012) Intraspinal rewiring of the corticospinal tract requires target-derived brain-derived neurotrophic factor and compensates lost function after brain injury. Brain 135:1253-1267. CrossRef Medline
48. Valverde F (1962) Reticular formation of the albino rat's brain stem cytoarchitecture and corticofugal connections. J Comp Neurol 119:25-53. CrossRef Medline
49. Welmer AK, Widén Holmqvist L, Sommerfeld DK (2010) Location and severity of spasticity in the first 1-2 weeks and at 3 and 18 months after stroke. Eur J Neurol 17:720-725. CrossRef Medline
50. Whishaw IQ (2004) The behavior of the laboratory rat. In:Ahandbook with tests. Oxford: Oxford UP.
51. Wiessner C, Bareyre FM, Allegrini PR, Mir AK, Frentzel S, Zurini M, Schnell L, Oertle T, Schwab ME (2003) Anti-Nogo-A antibody infusion 24 h after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J Cereb Blood Flow Metab 23:154-165. Medline
52. Woods JW (1964) Behavior of chronic decerebrate rats. J Neurophysiol 27: 635-644. Medline
53. Yoshikawa A, Atobe Y, Takeda A, Kamiya Y, Takiguchi M, Funakoshi K (2011) A retrograde tracing study of compensatory corticospinal projections in rats with neonatal hemidecortication. Dev Neurosci 33:539-547. CrossRef Medline
54. Zhao S, Zhao M, Xiao T, Jolkkonen J, Zhao C (2013) Constraint-induced movement therapy overcomes the intrinsic axonal growth-inhibitory signals in stroke rats. Stroke 44:1698-1705. CrossRef Medline