Role of IGF-1 in cortical plasticity and functional deficit induced by sensorimotor restriction

Behavioural Brain Research

Volumn 290, Issue , 2015, Pages 117-123

  Mysoet, Julien ^a,b   Dupont, Erwan ^a,b   Bastide, Bruno ^a,b   Canu, Marie Hélène ^a,b  

^a UNIVERSITÉ D'ARTOIS   (France)

^b UNIV LILLE   (France)

Author keywords

Adult rat; Cortical plasticity; Cutaneous receptive field; Disuse; Electrophysiology; Hindlimb unloading; Somatotopy; Tactile sensation; Von Frey monofilament

Indexed keywords

SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; BRAIN MAPPING; CONTROLLED STUDY; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; HINDLIMB; HINDLIMB UNLOADING; HYPOACTIVITY; MALE; NERVE CELL PLASTICITY; NONHUMAN; OSMOTIC MINIPUMP; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTIVE FIELD; SENSORIMOTOR FUNCTION; SKIN SENSITIVITY; SOMATOSENSORY CORTEX; SOMATOTOPIC MAP; STIMULUS RESPONSE; TACTILE DISCRIMINATION; WITHDRAWAL REFLEX; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; IMMOBILIZATION; METABOLISM; PATHOPHYSIOLOGY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; SENSORY DEPRIVATION; TOUCH; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; DISCRIMINATION (PSYCHOLOGY); HINDLIMB SUSPENSION; INSULIN-LIKE GROWTH FACTOR I; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SENSORY DEPRIVATION; SENSORY THRESHOLDS; SOMATOSENSORY CORTEX; TOUCH;

EID: 84929307446     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.04.055     Document Type: Article

References (48)

1. Bondy C.a., Cheng C.M. Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol 2004, 10.1016/j.ejphar.2004.02.042.
2. Bouet V., Boulouard M., Toutain J., Divoux D., Bernaudin M., Schumann-Bard P., et al. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009, 4:1560-1564. 10.1038/nprot.2009.125.
3. Canu M.H., Falempin M. Effect of hindlimb unloading on interlimb coordination during treadmill locomotion in the rat. Eur J Appl Physiol Occup Physiol 1996, 78:509-515. 10.1007/s004210050453.
4. Canu M.H., Garnier C. A 3D analysis of fore- and hindlimb motion during overground and ladder walking: Comparison of control and unloaded rats. Exp Neurol 2009, 218:98-108. 10.1016/j.expneurol.2009.04.009.
5. Canu M.H., Treffort N., Picquet F., Dubreucq G., Guerardel Y., Falempin M. Concentration of amino acid neurotransmitters in the somatosensory cortex of the rat after surgical or functional deafferentation. Exp Brain Res 2006, 173:623-628. 10.1007/s00221-006-0401-2.
6. Carro E., Nuñez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000, 20:2926-2933. 10.1016/j.tins.2006.06.011.
7. Clark B.C., Manini T.M., Bolanowski S.J., Ploutz-Snyder L.L. Adaptations in human neuromuscular function following prolonged unweighting: II. Neurological properties and motor imagery efficacy. J Appl Physiol 2006, 101:264-272. 10.1152/japplphysiol.01404.2005.
8. Coq J.O., Xerri C. Tactile impoverishment and sensorimotor restriction deteriorate the forepaw cutaneous map in the primary somatosensory cortex of adult rats. Exp Brain Res 1999, 129:518-531. 10.1007/s002210050922.
9. D'Amelio F., Fox R.a., Wu L.C., Daunton N.G. Quantitative changes of GABA-immunoreactive cells in the hindlimb representation of the rat somatosensory cortex after 14-day hindlimb unloading by tail suspension. J Neurosci Res 1996, 44:532-539. 10.1002/(SICI)1097-4547(19960615)44:6<532::AID-JNR3>3.0.CO;2-C.
10. De la Monte S.M., Wands J.R. Review of insulin and insulin-like growth factor expression, signaling, and malfunction in the central nervous system: relevance to Alzheimer's disease. J Alzheimers Dis 2005, 7:45-61.
11. De Meyts P. Insulin and its receptor: Structure, function and evolution. BioEssays 2004, 10.1002/bies.20151.
12. Ding Q., Vaynman S., Akhavan M., Ying Z., Gomez-Pinilla F. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2006, 140:823-833. 10.1016/j.neuroscience.2006.02.084.
13. Dupont E., Canu M.H., Falempin M. Atropine prevents the changes in the hindlimb cortical area induced by hypodynamia-hypokinesia. Brain Res 2002, 926:51-57. 10.1016/S0006-8993(01)03293-0.
14. Dupont E., Canu M.H., Falempin M. A 14- day period of hindpaw sensory deprivation enhances the responsiveness of rat cortical neurons. Neuroscience 2003, 121:433-439. 10.1016/S0306-4522(03)00494-9.
15. Dupont E., Canu M.H., Stevens L., Falempin M. Effects of a 14-day period of hindpaw sensory restriction on mRNA and protein levels of NGF and BDNF in the hindpaw primary somatosensory cortex. Mol Brain Res 2005, 133:78-86. 10.1016/j.molbrainres.2004.09.019.
16. Dupont E., Stevens L., Cochon L., Falempin M., Bastide B., Canu M.H. Erk is involved in the reorganization of somatosensory cortical maps in adult rats submitted to hindlimb unloading. PLoS One 2011, 6. 10.1371/journal.pone.0017564.
17. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can J Physiol Pharmacol 1997, 75:535-545. 10.1139/y97-089.
18. Fernandez A.M., Torres-Alemán I. The many faces of insulin-like peptide signalling in the brain. Nat Rev Neurosci 2012, 10.1038/nrn3209.
19. Flück M., Hoppeler H. Molecular basis of skeletal muscle plasticity--from gene to form and function. Rev Physiol Biochem Pharmacol 2003, 146:159-216. 10.1007/s10254-002-0004-7.
20. Fortney S.M., Schneider V.S., Greenleaf J.E. The physiology of bed rest. Handbook of Physiology, section 4, Environmental Physiology 1996, 889-939. Oxford University Press, New York. M.J. Fregly, C.M. Blatteis (Eds.).
21. Gatti R., De Palo E.F., Antonelli G., Spinella P. IGF-I/IGFBP system: metabolism outline and physical exercise. J Endocrinol Invest 2012, 35:699-707. 10.3275/8456.
22. Huber R., Ghilardi M.F., Massimini M., Ferrarelli F., Riedner B.a., Peterson M.J., et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci 2006, 9:1169-1176. 10.1038/nn1758.
23. Kano M., Iino K., Kano M. Functional reorganization of adult cat somatosensory cortex is dependent on NMDA receptors. Neuroreport 1991, 2:77-80. 10.1097/00001756-199102000-00003.
24. Langlet C., Canu M.H., Falempin M. Short-term reorganization of the rat somatosensory cortex following hypodynamia-hypokinesia. Neurosci Lett 1999, 266:145-148. 10.1016/S0304-3940(99)00296-7.
25. Lissek S., Wilimzig C., Stude P., Pleger B., Kalisch T., Maier C., et al. Immobilization impairs tactile perception and shrinks somatosensory cortical maps. Curr Biol 2009, 19:837-842. 10.1016/j.cub.2009.03.065.
26. Llorens-Martín M., Torres-Alemán I., Trejo J.L. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behaviour. Mol Cell Neurosci 2010, 44:109-117. 10.1016/j.mcn.2010.02.006.
27. Martinez M., Brezun J.M., Zennou-Azogui Y., Baril N., Xerri C. Sensorimotor training promotes functional recovery and somatosensory cortical map reactivation following cervical spinal cord injury. Eur J Neurosci 2009, 30:2356-2367. 10.1111/j. 1460-9568.2009.07019.x.
28. Maya-Vetencourt J.F., Baroncelli L., Viegi A., Tiraboschi E., Castren E., Cattaneo A., et al. IGF-1 restores visual cortex plasticity in adult life by reducing local GABA levels. Neural Plast 2012, 201:2. 10.1155/2012/250421.
29. Morey-Holton E.R., Globus R.K. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 2002, 92:1367-1377. 10.1152/japplphysiol.00969.2001.
30. Mysoet J., Canu M.-H., Cieniewski-Bernard C., Bastide B., Dupont E. Hypoactivity affects IGF-1 Level and PI3K/AKT signaling pathway in cerebral structures implied in motor control. PLoS One 2014, 9:e107631. 10.1371/journal.pone.0107631.
31. Niblock M.M., Brunso-Bechtold J.K., Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci 2000, 20:4165-4176.
32. Nishijima T., Piriz J., Duflot S., Fernandez A.M., Gaitan G., Gomez-Pinedo U., et al. Neuronal activity drives localized blood-brain-barrier transport of serum insulin-like growth factor-i into the CNS. Neuron 2010, 67:834-846. 10.1016/j.neuron.2010.08.007.
33. Nuñez A., Carro E.G., Torres-Aleman I. Insulin-like growth factor I modifies electrophysiological properties of rat brain stem neurons. J Neurophysiol 2003, 89:3008-3017. 10.1152/jn.00089.2003.
34. Pitcher G.M., Ritchie J., Henry J.L. Paw withdrawal threshold in the von Frey hair test is influenced by the surface on which the rat stands. J Neurosci Methods 1999, 87:185-193. 10.1016/S0165-0270(99)00004-7.
35. Ploughman M., Windle V., MacLellan C.L., White N., Doré J.J., Corbett D. Brain-derived neurotrophic factor contributes to recovery of skilled reaching after focal ischemia in rats. Strok 2009, 40:1490-1495. 10.1161/STROKEAHA.108.531806.
36. Roberts D.R., Ramsey D., Johnson K., Kola J., Ricci R., Hicks C., et al. Cerebral cortex plasticity after 90 days of bed rest: Data from TMS and fMRI. Aviat Sp Environ Med 2010, 81:30-40. 10.3357/ASEM.2532.2009.
37. Rosselet C., Zennou-Azogui Y., Xerri C. Nursing-induced somatosensory cortex plasticity: temporally decoupled changes in neuronal receptive field properties are accompanied by modifications in activity-dependent protein expression. J Neurosci 2006, 26:10667. 10.1523/JNEUROSCI. 3253-06.2006.
38. Schäbitz W.R., Steigleder T., Cooper-Kuhn C.M., Schwab S., Sommer C., Schneider A., et al. Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Strok 2007, 38:2165-2172. 10.1161/STROKEAHA.106.477331.
39. Schwarz A.J., Brasel J.A., Hintz R.L., Mohan S., Cooper D.M. Acute effect of brief low- and high-intensity exercise on circulating insulin-like growth factor (IGF) I, II, and IGF-binding protein-3 and its proteolysis in young healthy men. J Clin Endocrinol Metab 1996, 81:3492-3497. 10.1210/jc.81.10.3492.
40. Tegenthoff M., Ragert P., Pleger B., Schwenkreis P., Förster A.F., Nicolas V., et al. Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5Hz rTMS. PLoS Biol 2005, 3:2031-2040. 10.1371/journal.pbio.0030362.
41. Torres-Aleman I. Toward a comprehensive neurobiology of IGF-I. Dev Neurobiol 2010, 10.1002/dneu.20778.
42. Viguier M., Dupui P., Montoya R. Posture analysis on young women before and after 60 days of -6?? head down bed rest. Gait Posture 2005, 29:188-193. 10.1016/j.gaitpost.2008.08.001.
43. Wan Q., Xiong Z.G., Man H.Y., Ackerley C.A., Braunton J., Lu W.Y., et al. Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 1997, 388:686-690. 10.1038/41792.
44. Wang Q., Liu L., Pei L., Ju W., Ahmadian G., Lu J., et al. Control of synaptic strength, a novel function of Akt. Neuron 2003, 38:915-928. 10.1016/S0896-6273(03)00356-8.
45. Weibull A., Flondell M., Rosén B., Björkman A. Cerebral and clinical effects of short-term hand immobilisation. Eur J Neurosci 2011, 33:699-704. 10.1111/j. 1460-9568.2010.07551.x.
46. Westwood A.J., Beiser A., Decarli C., Harris T.B., Chen T.C., He X.-M., et al. Insulin-like growth factor-1 and risk of Alzheimer dementia and brain atrophy. Neurology 2014, 82:1613-1619. 10.1212/WNL.0000000000000382.
47. Xerri C., Bourgeon S., Coq J.O. Perceptual context-dependent remodeling of the forepaw map in the SI cortex of rats trained on tactile discrimination. Behav Brain Res 2005, 162:207-221. 10.1016/j.bbr.2005.03.003.
48. Xing C., Yin Y., Chang R., Gong X., He X., Xie Z. Effects of insulin-like growth factor 1 on synaptic excitability in cultured rat hippocampal neurons. Exp Neurol 2007, 205:222-229. 10.1016/j.expneurol.2007.01.029.