Chronic in vivo imaging shows no evidence of dendritic plasticity or functional remapping in the contralesional cortex after stroke

Cerebral Cortex

Volumn 23, Issue 4, 2013, Pages 751-762

  Johnston, David G ^a,b   Denizet, Marie ^a,c   Mostany, Ricardo ^a   Portera Cailliau, Carlos ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Neuroscience Interdepartmental Program and   (United States)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

2 photon; intrinsic optical signal imaging; ischemia; middle cerebral artery occlusion; rose Bengal

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; CELL GROWTH; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CONVALESCENCE; DENDRITIC CELL; FEMALE; HEMISPHERE; IMAGE ANALYSIS; IN VIVO STUDY; MALE; MICROSCOPE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; MULTIPHOTON MICROSCOPY; NERVE CELL PLASTICITY; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SURVIVOR;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN MAPPING; CEREBRAL CORTEX; DENDRITES; DISEASE MODELS, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; GREEN FLUORESCENT PROTEINS; LONGITUDINAL STUDIES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEURONAL PLASTICITY; PYRAMIDAL CELLS; STROKE;

EID: 84875144043     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs092     Document Type: Article

References (65)

1. Abo M, Chen Z, Lai LJ, Reese T, Bjelke B. 2001. Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. Neuroreport. 12:1543-1547.
2. Biernaskie J, Chernenko G, Corbett D. 2004. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci. 24:1245-1254.
3. Brown CE, Aminoltejari K, Erb H, Winship IR, Murphy TH. 2009. In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J Neurosci. 29:1719-1734.
4. Brown CE, Li P, Boyd JD, Delaney KR, Murphy TH. 2007. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci. 27:4101-4109.
5. Calautti C, Baron JC. 2003. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke. 34:1553-1566.
6. Calautti C, Leroy F, Guincestre JY, Marie RM, Baron JC. 2001. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport. 12:3883-3886.
7. Cao Y, George KP, Ewing JR, Vikingstad EM, Johnson AF. 1998. Neuroimaging of language and aphasia after stroke. J Stroke Cerebrovasc Dis. 7:230-233.
8. Carey JR, Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey L, Rundquist P, Ugurbil K. 2002. Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain. 125:773-788.
9. Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS. 1991. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 29:63-71.
10. Cramer SC, Crafton KR. 2006. Somatotopy and movement representation sites following cortical stroke. Exp Brain Res. 168:25-32.
11. deVeber GA, MacGregor D, Curtis R, Mayank S. 2000. Neurologic outcome in survivors of childhood arterial ischemic stroke and sinovenous thrombosis. J Child Neurol. 15:316-324.
12. Devor A, Hillman EM, Tian P, Waeber C, Teng IC, Ruvinskaya L, Shalinsky MH, Zhu H, Haslinger RH, Narayanan SN, et al. 2008. Stimulus-induced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J Neurosci. 28:14347-14357.
13. Diamond ME, Petersen RS, Harris JA. 1999. Learning through maps: functional significance of topographic organization in primary sensory cortex. J Neurobiol. 41:64-68.
14. Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, Rosen BR, Finklestein SP. 2001. Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci U S A. 98:12766-12771.
15. Dijkhuizen RM, Singhal AB, Mandeville JB, Wu O, Halpern EF, Finklestein SP, Rosen BR, Lo EH. 2003. Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J Neurosci. 23:510-517.
16. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron. 28:41-51.
17. Forgie ML, Gibb R, Kolb B. 1996. Unilateral lesions of the forelimb area of rat motor cortex: lack of evidence for use-dependent neural growth in the undamaged hemisphere. Brain Res. 710: 249-259.
18. Fujii Y, Nakada T. 2003. Cortical reorganization in patients with subcortical hemiparesis: neural mechanisms of functional recovery and prognostic implication. J Neurosurg. 98:64-73.
19. Ganesan V, Hogan A, Shack N, Gordon A, Isaacs E, Kirkham FJ. 2000. Outcome after ischaemic stroke in childhood. Dev Med Child Neurol. 42:455-461.
20. Gibb RL, Gonzalez CL, Wegenast W, Kolb BE. 2010. Tactile stimulation promotes motor recovery following cortical injury in adult rats. Behav Brain Res. 214:102-107.
21. Glees P, Cole J. 1950. Recovery of skilled motor functions after small repeated lesions of motor cortex in macaque. J Neurophysiol. 13:137-148.
22. Grotta JC, Jacobs TP, Koroshetz WJ, Moskowitz MA. 2008. Stroke program review group: an interim report. Stroke. 39:1364-1370.
23. Grove EA, Fukuchi-Shimogori T. 2003. Generating the cerebral cortical area map. Annu Rev Neurosci. 26:355-380.
24. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M. 2009. Experience leaves a lasting structural trace in cortical circuits. Nature. 457:313-317.
25. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hubener M, Keck T, Knott G, Lee WC, et al. 2009. Longterm, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc. 4:1128-1144.
26. Holtmaat A, Svoboda K. 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci. 10:647-658.
27. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. 2006. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature. 441:979-983.
28. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K. 2005. Transient and persistent dendritic spines in the neocortex in vivo. Neuron. 45:279-291.
29. Johnston MV. 2009. Plasticity in the developing brain: implications for rehabilitation. Dev Disabil Res Rev. 15:94-101.
30. Jones TA, Schallert T. 1992. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Res. 581:156-160.
31. Jones TA, Schallert T. 1994. Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci. 14:2140-2152.
32. Kim CT, Han J, Kim H. 2009. Pediatric stroke recovery: a descriptive analysis. Arch Phys Med Rehabil. 90:657-662.
33. Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E. 2006. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol. 4:e29.
34. Lim D, Mohajerani M, LeDue J, Boyd J, Chen S, Murphy T. 2012. In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas. Front Neural Circuits. 6:11.
35. Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, et al. 2009. Heart disease and stroke statistics-2009 update: a report from the American Heart Association statistics Committee and stroke statistics Subcommittee. Circulation. 119:480-486.
36. Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C. 2006. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci. 26:6096-6102.
37. Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL. 2000. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke. 31:656-661.
38. Mohajerani MH, Aminoltejari K, Murphy TH. 2011. Targeted ministrokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc Natl Acad Sci U S A. 108:E183-E191.
39. Mostany R, Chowdhury TG, Johnston DG, Portonovo SA, Carmichael ST, Portera-Cailliau C. 2010. Local hemodynamics dictate long-term dendritic plasticity in peri-infarct cortex. J Neurosci. 30:14116-14126.
40. Mostany R, Portera-Cailliau C. 2008. A craniotomy surgery procedure for chronic brain imaging. J Vis Exp. (12):pii: 680.
41. Mostany R, Portera-Cailliau C. 2011. Absence of large-scale dendritic plasticity of layer 5 pyramidal neurons in peri-infarct cortex. J Neurosci. 31:1734-1738.
42. Murphy TH, Corbett D. 2009. Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci. 10:861-872.
43. Pologruto TA, Sabatini BL, Svoboda K. 2003. ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online. 2:13.
44. Prusky G, Whishaw IQ. 1996. Morphology of identified corticospinal cells in the rat following motor cortex injury: absence of usedependent change. Brain Res. 714:1-8.
45. Roof RL, Schielke GP, Ren X, Hall ED. 2001. A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke. 32:2648-2657.
46. Rossini PM, Calautti C, Pauri F, Baron JC. 2003. Post-stroke plastic reorganisation in the adult brain. Lancet Neurol. 2:493-502.
47. Schaechter JD, Perdue KL. 2008. Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb Cortex. 18:638-647.
48. Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ. 1998. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol. 55:1081-1088.
49. Skilbeck CE, Wade DT, Hewer RL, Wood VA. 1983. Recovery after stroke. J Neurol Neurosurg Psychiatry. 46:5-8.
50. Takatsuru Y, Fukumoto D, Yoshitomo M, Nemoto T, Tsukada H, Nabekura J. 2009. Neuronal circuit remodeling in the contralateral cortical hemisphere during functional recovery from cerebral infarction. J Neurosci. 29:10081-10086.
51. Tamura A, Graham DI, McCulloch J, Teasdale GM. 1981. Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab. 1:53-60.
52. Tennant KA, Jones TA. 2009. Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. J Neurosci Methods. 181:18-26.
53. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. 2002. Long-term in vivo imaging of experiencedependent synaptic plasticity in adult cortex. Nature. 420: 788-794.
54. Tuor UI, Wang R, Zhao Z, Foniok T, Rushforth D, Wamsteeker JI, Qiao M. 2007. Transient hypertension concurrent with forepaw stimulation enhances functional MRI responsiveness in infarct and peri-infarct regions. J Cereb Blood Flow Metab. 27:1819-1829.
55. Twitchell TE. 1951. The restoration of motor function following hemiplegia in man. Brain. 74:443-480.
56. Van der Gucht E, Hof PR, Van Brussel L, Burnat K, Arckens L. 2007. Neurofilament protein and neuronal activity markers define regional architectonic parcellation in the mouse visual cortex. Cereb Cortex. 17:2805-2819.
57. Ward NS. 2004. Functional reorganization of the cerebral motor system after stroke. Curr Opin Neurol. 17:725-730.
58. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD. 1985. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol. 17:497-504.
59. Weber R, Ramos-Cabrer P, Justicia C, Wiedermann D, Strecker C, Sprenger C, Hoehn M. 2008. Early prediction of functional recovery after experimental stroke: functional magnetic resonance imaging, electrophysiology, and behavioral testing in rats. J Neurosci. 28:1022-1029.
60. Weiller C, Chollet F, Friston KJ, Wise RJ, Frackowiak RS. 1992. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol. 31:463-472.
61. Wilbrecht L, Holtmaat A, Wright N, Fox K, Svoboda K. 2010. Structural plasticity underlies experience-dependent functional plasticity of cortical circuits. J Neurosci. 30:4927-4932.
62. Winship IR, Murphy TH. 2008. In vivo calcium imaging reveals functional rewiring of single somatosensory neurons after stroke. J Neurosci. 28:6592-6606.
63. Witte OW, Bidmon HJ, Schiene K, Redecker C, Hagemann G. 2000. Functional differentiation of multiple perilesional zones after focal cerebral ischemia. J Cereb Blood Flow Metab. 20:1149-1165.
64. Zhang ZG, Chopp M. 2009. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol. 8:491-500.
65. Zuo Y, Lin A, Chang P, Gan WB. 2005. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron. 46:181-189.