Adaptive changes in the motor cortex during and after longterm forelimb immobilization in adult rats

Journal of Physiology

Volumn 592, Issue 10, 2014, Pages 2137-2152

  Viaro, Riccardo ^a,b   Budri, Mirco ^a   Parmiani, Pierantonio ^a   Franchi, Gianfranco ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CAST REMOVAL; CONTROLLED STUDY; FORELIMB; IMMOBILIZATION; LIMB MOVEMENT; MALE; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RAT; ROTAROD TEST; SYNAPTIC TRANSMISSION; ADAPTATION; ANIMAL; MOTOR ACTIVITY; MOTOR CORTEX; NERVE CELL INHIBITION; PHYSIOLOGY; WISTAR RAT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; FORELIMB; HINDLIMB SUSPENSION; IMMOBILIZATION; MALE; MOTOR ACTIVITY; MOTOR CORTEX; NEURAL INHIBITION; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 84900497620     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.268821     Document Type: Article

References (60)

1. Bonazzi L, Viaro R, Lodi E, Canto R, Bonifazzi C & Franchi G (2013). Complex movement topography and extrinsic space representation in the rat forelimb motor cortex as defined by long-duration intracortical microstimulation. J Neurosci 33, 2097-2107.
2. Clark BC, Issac LC, Lane JL, Damron LA & Hoffman RL (2008). Neuromuscular plasticity during and following 3 wk of human forearm cast immobilization. J Appl Physiol 105, 868-878.
3. Clark BC, Taylor JL, Hoffman RL, Dearth DJ & Thomas JS (2010). Cast immobilization increases long-interval intracortical inhibition. Muscle Nerve 42, 363-372.
4. Cohen LG, Bandinelli S, Findley TW & Hallett M (1991). Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. Brain 114, 615-627.
5. Coq JO, Barr AE, Strata F, Russier M, Kietrys DM, Merzenich MM, Byl NN & Barbe MF (2009). Peripheral and central changes combine to induce motor behavioral deficits in a moderate repetition task. Exp Neurol 220, 234-245.
6. Coq JO & Xerri C (1999). Tactile impoverishment and sensorimotor restriction deteriorate the forepaw cutaneous map in the primary somatosensory cortex of adult rats. Exp Brain Res 129, 518-531.
7. Dombeck DA, Graziano MS & Tank DW (2009). Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice. J Neurosci 29, 13751-13760.
8. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
9. Elbert T, Pantev C, Wienbruch C, Rockstroh B & Taub E (1995). Increased cortical representation of the fingers of the left hand in string players. Science 270, 305-307.
10. Fox K & Wong RO (2005). A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48, 465-477.
11. Franchi G (2000). Reorganization of vibrissal motor representation following severing and repair of the facial nerve in adult rats. Exp Brain Res 131, 33-43.
12. Franchi G (2002). Time course of motor cortex reorganization following botulinum toxin injection into the vibrissal pad of the adult rat. Eur J Neurosci 16, 1333-1348.
13. Friedberg MH, Lee SM & Ebner FF (1999). Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anaesthesia. J Neurophysiol 81, 2243-2252.
14. Fu M & Zuo Y (2011). Experience-dependent structural plasticity in the cortex. Trends Neurosci 34, 177-187.
15. Giszter S, Davies MR, Ramakrishnan A, Udoekwere UI & Kargo WJ (2008). Trunk sensorimotor cortex is essential for autonomous weight-supported locomotion in adult rats spinalized as P1/P2 neonates. J Neurophysiol 100, 839-851.
16. Ghosh S, Laxmi TR & Chattarji S (2013). Functional connectivity from the amygdala to the hippocampus grows stronger after stress. J Neurosci 33, 7234-7244.
17. Henderson AK, Pittman QJ & Teskey GC (2012). High frequency stimulation alters motor maps, impairs skilled reaching performance and is accompanied by an upregulation of specific GABA, glutamate and NMDA receptor subunits. Neuroscience 215, 98-113.
18. Hira R, Ohkubo F, Tanaka YR, Masamizu Y, Augustine GJ, Kasai H & Matsuzaki M (2013). In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas. Front Neural Circuits 7, 55.
19. Jacobs KM & Donoghue JP (1991). Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251, 944-945.
20. Jones TA & Schallert T (1994). Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci 14, 2140-2152.
21. Kao T, Shumsky JS, Knudsen EB, Murray M & Moxon KA (2011). Functional role of exercise-induced cortical organization of sensorimotor cortex after spinal transection. J Neurophysiol 106, 2662-2674.
22. Kim U & Lee T (2013). Intra-areal and corticocortical circuits arising in the disgranular zone of rat primary somatosensory cortex that processes deep input. J Comp Neurol 521, 2585-2601.
23. Kleim JA, Barbay S & Nudo RJ (1998). Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80, 3321-3325.
24. Langer N, Hänggi J, Müller NA, Simmen HP & Jäncke L (2012). Effects of limb immobilization on brain plasticity. Neurology 78, 182-188.
25. Langlet C, Bastide B & Canu MH (2012). Hindlimb unloading affects cortical motor maps and decreases corticospinal excitability. Exp Neurol 237, 211-217.
26. Leingärtner A, Thuret S, Kroll TT, Chou SJ, Leasure JL, Gage FH & O'Leary DD (2007). Cortical area size dictates performance at modality-specific behaviors. Proc Natl Acad Sci U S A 104, 4153-4158.
27. Liepert J, Tegenthoff M & Malin JP (1995). Changes of cortical motor area size during immobilization. Electroencephalogr Clin Neurophysiol 97, 382-386.
28. Lissek S, Wilimzig C, Stude P, Pleger B, Kalisch T, Maier C, Peters SA, Nicolas V, Tegenthoff M & Dinse HR (2009). Immobilization impairs tactile perception and shrinks somatosensory cortical maps. Curr Biol 19, 837-842.
29. Maggiolini E, Viaro R & Franchi G (2008). Suppression of activity in the forelimb motor cortex temporarily enlarges forelimb representation in the homotopic cortex in adult rats. Eur J Neurosci 27, 2733-2746.
30. Marti M, Mela F, Fantin M, Zucchini S, Brown JM, Witta J, Di Benedetto M, Buzas B, Reinscheid RK, Salvadori S, Guerrini R, Romualdi P, Candeletti S, Simonato M, Cox BM & Morari M (2005). Blockade of nociceptin/orphanin FQ transmission attenuates symptoms and neurodegeneration associated with Parkinson's disease. J Neurosci 25, 9591-9601.
31. Milliken GW, Plautz EJ & Nudo RJ (2013). Distal forelimb representations in primary motor cortex are redistributed after forelimb restriction: a longitudinal study in adult squirrel monkeys. J Neurophysiol 109, 1268-1282.
32. Molina-Luna K, Hertler B, Buitrago MM & Luft AR (2008). Motor learning transiently changes cortical somatotopy. Neuroimage 40, 1748-1754.
33. Neafsey EJ & Sievert C (1982). A second forelimb motor area exists in rat frontal cortex. Brain Res 232, 151-156.
34. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF & Terreberry RR (1986). The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396, 77-96.
35. Nudo RJ, Jenkins WM & Merzenich MM (1990). Repetitive microstimulation alters the cortical representation of movements in adult rats. Somatosens Mot Res 7, 463-483.
36. Nudo RJ, Milliken GW, Jenkins WM & Merzenich MM (1996). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16, 785-807.
37. Pascual-Leone A & Torres F (1993). Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 116, 39-52.
38. Petersen CC (2007). The functional organization of the barrel cortex. Neuron 56, 339-355.
39. Plautz EJ, Milliken GW & Nudo RJ (2000). Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74, 27-55.
40. Ramanathan D, Conner JM & Tuszynski MH (2006). A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc Natl Acad Sci U S A 103, 11370-11375.
41. Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V & Kilgard MP (2011). Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70, 121-131.
42. Roll R, Kavounoudias A, Albert F, Legré R, Gay A, Fabre B & Roll JP (2012). Illusory movements prevent cortical disruption caused by immobilization. Neuroimage 62, 510-519.
43. Rouiller EM, Moret V & Liang F (1993). Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. Somatosens Mot Res 10, 269-289.
44. Rozas G, Guerra MJ & Labandeira-Garcia JL (1997). An automated rotarod method for quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res Brain Res Protoc 2, 75-84.
45. Sanberg PR, Bunsey MD, Giordano M & Norman AB (1988). The catalepsy test: its ups and downs. Behav Neurosci 102, 748-759.
46. Sanes JN, Suner S & Donoghue JP (1990). Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term pattern of reorganization following motor or mixed peripheral nerve lesion. Exp Brain Res 79, 479-491.
47. Sanes JN & Donoghue JP (2000). Plasticity and primary motor cortex. Annu Rev Neurosci 23, 393-415.
48. Schneider C, Devanne H, Lavoie BA & Capaday C (2002). Neural mechanisms involved in the functional linking of motor cortical points. Exp Brain Res 146, 86-94.
49. Sterr A, Müller MM, Elbert T, Rockstroh B, Pantev C & Taub E (1998). Perceptual correlates of changes in cortical representation of fingers in blind multifinger Braille readers. J Neurosci 18, 4417-4423.
50. Stojic AS, Lane RD, Killackey HP & Rhoades RW (2000). Suppression of hindlimb inputs to S-I forelimb-stump representation of rats with neonatal forelimb removal: GABA receptor blockade and single-cell responses. J Neurophysiol 83, 3377-3387.
51. Teskey GC, Flynn C, Goertzen CD, Monfils MH & Young NA (2003). Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol Res 25, 794-800.
52. Toldi J, Laskawi R, Landgrebe M & Wolff JR (1996). Biphasic reorganization of somatotopy in the primary motor cortex follows facial nerve lesions in adult rats. Neurosci Lett 203, 179-182.
53. Toussaint L & Meugnot A (2013). Short-term limb immobilization affects cognitive motor processes. J Exp Psychol Learn Mem Cogn 39, 623-632.
54. Trinel D, Picquet F, Bastide B & Canu MH (2013). Dendritic spine remodeling induced by hindlimb unloading in adult rat sensorimotor cortex. Behav Brain Res 249, 1-7.
55. 3 receptor blockade. Exp Neurol 223, 473-484.
56. Viaro R, Morari M & Franchi G (2011). Progressive motor cortex functional reorganization following 6-hydroxydopamine lesioning in rats. J Neurosci 31, 4544-4554.
57. Wang L, Conner JM, Rickert J & Tuszynski MH (2011). Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain. Proc Natl Acad Sci U S A 108, 2545-2550.
58. Young NA, Vuong J, Flynn C & Teskey GC (2011). Optimal parameters for microstimulation derived forelimb movement thresholds and motor maps in rats and mice. J Neurosci Methods 196, 60-69.
59. Young NA, Vuong J & Teskey GC (2012). Development of motor maps in rats and their modulation by experience. J Neurophysiol 108, 1309-1317.
60. Zanette G, Manganotti P, Fiaschi A & Tamburin S (2004). Modulation of motor cortex excitability after upper limb immobilization. Clin Neurophysiol 115, 1264-1275.