Activity-dependent codevelopment of the corticospinal system and target interneurons in the cervical spinal cord

Journal of Neuroscience

Volumn 29, Issue 27, 2009, Pages 8816-8827

  Chakrabarty, Samit ^a   Shulman, Brandon ^a   Martin, John H ^a,b  

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

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN; CALRETININ; CHOLINE ACETYLTRANSFERASE; MUSCIMOL; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAT; CERVICAL SPINAL CORD; CONTROLLED STUDY; GRAY MATTER; IMMUNOHISTOCHEMISTRY; INTERNEURON; MOTOR DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL TRACT; SPINAL CORD MOTONEURON;

ACTION POTENTIALS; ANIMALS; CATS; CELL DIFFERENTIATION; CERVICAL VERTEBRAE; CHOLINE O-ACETYLTRANSFERASE; FEMALE; INTERNEURONS; NEUROGENESIS; PYRAMIDAL TRACTS; SPINAL CORD;

EID: 67650479289     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0735-09.2009     Document Type: Article

References (50)

1. Albuquerque C, Lee CJ, Jackson AC, MacDermott AB (1999) Subpopulations of GABAergic and non-GABAergic rat dorsal horn neurons express Ca2+-permeable AMPA receptors. Eur J Neurosci 11:2758-2766.
2. Alisky JM, Swink TD, Tolbert DL (1992) The postnatal spatial and temporal development of corticospinal projections in cats. Exp Brain Res 88:265-276.
3. Alstermark B, Ohlson S (2000) Origin of corticospinal neurones evoking monosynaptic excitation in C3-C4 propriospinal neurones in the cat. Neurosci Res 38:249-256.
4. Anelli R, Heckman CJ (2005) The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord. J Neurocytol 34:369-385.
5. Armand J, Holstege G, Kuypers HG (1985) Differential corticospinal projections in the cat. An autoradiographic tracing study. Brain Res 343:351-355.
6. Armand J, Olivier E, Edgley SA, Lemon RN (1997) Postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey. J Neurosci 17:251-266.
7. Bruce IC, Tatton WG (1980) Synchronous development of motor cortical output to different muscles in the kitten. Exp Brain Res 40:349-353.
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.
9. Celio MR, Baier W, Schärer L, de Viragh PA, Gerday C (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81-86.
10. Chakrabarty S, Martin JH (2000) Postnatal development of the motor representation in primary motor cortex. J Neurophysiol 84:2582-2594.
11. Chakrabarty S, Friel KM, Martin JH (2009) Activity-dependent plasticity improves M1 motor representation and corticospinal tract connectivity. J Neurophysiol 101:1283-1293.
12. Clowry GJ (2007) The dependence of spinal cord development on corticospinal input and its significance in understanding and treating spastic cerebral palsy. Neurosci Biobehav Rev 31:1114-1124.
13. Clowry GJ, Arnott GA, Clement-Jones M, Fallah Z, Gould S, Wright C (2000) Changing pattern of expression of parvalbumin immunoreactivity during human fetal spinal cord development. J Comp Neurol 423:727-735.
14. Clowry GJ, Davies BM, Upile NS, Gibson CL, Bradley PM (2004) Spinal cord plasticity in response to unilateral inhibition of the rat motor cortex during development: changes to gene expression, muscle afferents and the ipsilateral corticospinal projection. Eur J Neurosci 20:2555-2566.
15. Friel KM, Martin JH (2005) Role of sensory-motor cortex activity in postnatal development of corticospinal axon terminals in the cat. J Comp Neurol 485:43-56.
16. Friel KM, Martin JH (2007) Bilateral activity-dependent interactions in the developing corticospinal system. J Neurosci 27:11083-11090.
17. Friel KM, Drew T, Martin JH (2007) Differential activity-dependent development of corticospinal control of movement and final limb position during visually-guided locomotion. J Neurophysiol 97:3396-3406.
18. Gibson CL, Arnott GA, Clowry GJ (2000) Plasticity in the rat spinal cord seen in response to lesions to the motor cortex during development but not to lesions in maturity. Exp Neurol 166:422-434.
19. Giehl KM (2001) Trophic dependencies of rodent corticospinal neurons. Rev Neurosci 12:79-94.
20. Gonzalez-Forero D, Pastor AM, Geiman EJ, Benítez-Temiño B, Alvarez FJ (2005) Regulation of gephyrin cluster size and inhibitory synaptic currents on Renshaw cells by motor axon excitatory inputs. J Neurosci 25:417-429.
21. Hellström J, Oliveira AL, Meister B, Cullheim S (2003) Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J Comp Neurol 460:476-486.
22. Huang A, Noga BR, Carr PA, Fedirchuk B, Jordan LM (2000) Spinal cholinergic neurons activated during locomotion: localization and electrophysiological characterization. J Neurophysiol 83:3537-3547.
23. Kubota Y, Jones EG (1993) Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex. Brain Res 600:339-344.
24. Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195-218.
25. Li Q, Martin JH (2000) Postnatal development of differential projections from the caudal and rostral motor cortex subregions. Exp Brain Res 134:187-198.
26. Li Q, Martin JH (2001) Postnatal development of corticospinal axon terminal morphology in the cat. J Comp Neurol 435:127-141.
27. Martin J, Chakrabarty S (2008) Early postnatal co-development of corticospinal and proprioceptive circuits in the spinal cord. Soc Neurosci Abstr 34:29.12.
28. Martin J, Friel K, Salimi I, Chakrabarty S (2009) Corticospinal development. In: Encyclopedia of neuroscience (Squire L, ed), pp 203-214. Oxford: Academic.
29. Martin JH (1996) Differential spinal projections from the forelimb areas of the rostral and caudal subregions of primary motor cortex in the cat. Exp Brain Res 108:191-205.
30. Martin JH, Lee SJ (1999) Activity-dependent competition between developing corticospinal terminations. Neuroreport 10:2277-2282.
31. Martin JH, Kably B, Hacking A (1999) Activity-dependent development of cortical axon terminations in the spinal cord and brain stem. Exp Brain Res 125:184-199.
32. Martin JH, Donarummo L, Hacking A (2000) Impairments in prehension produced by early postnatal sensorimotor cortex activity blockade. J Neurophysiol 83:895-906.
33. Martin JH, Choy M, Pullman S, Meng Z (2004) Corticospinal development depends on experience. J Neurosci 24:2122-2132.
34. Martin P, Bateson P (1985) The ontogeny of locomotor play behavior in the domestic cat. Anim Behav 33:502-510.
35. Meng Z, Li Q, Martin JH (2004) The transition from development to motor control function in the corticospinal system. J Neurosci 24:605-614.
36. Miles GB, Hartley R, Todd AJ, Brownstone RM (2007) Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 104:2448-2453.
37. Monfils MH, Plautz EJ, Kleim JA (2005) In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11:471-483.
38. Phelps PE, Barber RP, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) Postnatal development of neurons containing choline acetyltransferase in rat spinal cord: an immunocytochemical study. J Comp Neurol 229:347-361.
39. Porter R, Lemon R (1993) Corticospinal function and voluntary movement. Oxford: Oxford Science.
40. Rexed B (1954) The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 100:297-379.
41. Salimi I, Friel KM, Martin JH (2008) Pyramidal tract stimulation restores normal corticospinal tract connections and visuomotor skill after early postnatal motor cortex activity blockade. J Neurosci 28:7426-7434.
42. Schoen JH (1964) Comparative aspects of the descending fibre systems in the spinal cord. Prog Brain Res 11:203-222.
43. Schwaller B, Meyer M, Schiffmann S (2002) 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241-258.
44. Spitzer NC, Borodinsky LN (2008) Implications of activity-dependent neurotransmitter-receptor matching. Philos Trans R Soc Lond B Biol Sci 363:1393-1399.
45. Theriault E, Tatton WG (1989) Postnatal redistribution of pericruciate motor cortical projections within the kitten spinal cord. Brain Res Dev Brain Res 45:219-237.
46. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
47. Verburgh CA, Kuypers HG, Voogd J, Stevens HP (1989) Spinocerebellar neurons and propriospinal neurons in the cervical spinal cord: a fluorescent double-labeling study in the rat and the cat. Exp Brain Res 75:73-82.
48. Villablanca JR, Olmstead CE (1979) Neurological development of kittens. Dev Psychobiol 12:101-127.
49. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
50. Wilson JM, Rempel J, Brownstone RM (2004) Postnatal development of cholinergic synapses on mouse spinal motoneurons. J Comp Neurol 474:13-23.