Ministrokes in channelrhodopsin-2 transgenic mice reveal widespread deficits in motor output despite maintenance of cortical neuronal excitability

Journal of Neuroscience

Volumn 34, Issue 4, 2014, Pages 1094-1104

  Anenberg, Eitan ^a,b   Arstikaitis, Pamela ^a,b   Niitsu, Yoichi ^a,b   Harrison, Thomas C ^a,b   Boyd, Jamie D ^a,b   Hilton, Brett J ^a   Tetzlaff, Wolfram ^a   Murphy, Timothy H ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Channelrhodopsin 2; Motor mapping; Mouse; Optogenetics; Plasticity; Stroke

Indexed keywords

CHANNELRHODOPSIN-2; MOTOR-MAPPING; MOUSE; OPTOGENETICS; PLASTICITY; STROKE;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; FEMALE; MALE; MICE; MICE, TRANSGENIC; MOTOR CORTEX; NEURONS; OPTOGENETICS; RECOVERY OF FUNCTION; RHODOPSIN; STROKE;

EID: 84892772158     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1442-13.2014     Document Type: Article

References (83)

1. Alaverdashvili M, Whishaw IQ (2010) Compensation aids skilled reaching in aging and in recovery from forelimb motor cortex stroke in the rat. Neuroscience 167:21-30. CrossRef Medline
2. Anderson CT, Sheets PL, Kiritani T, Shepherd GM G (2010) Sublayerspecific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat Neurosci 13:739-744. CrossRef Medline
3. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Feng G (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54:205-218. CrossRef Medline
4. + at critical levels of brain ischemia. Stroke 8:51-57. CrossRef Medline
5. Astrup J, Siesjö BK, Symon L (1981) Thresholds in cerebral ischemia-the ischemic penumbra. Stroke 12:723-725. CrossRef Medline
6. Ayling OGS, Harrison TC, Boyd JD, Goroshkov A, Murphy TH (2009) Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat Methods 6:219-224. CrossRef Medline
7. Baron JC (2001) Perfusion thresholds in human cerebral ischemia: historical perspective and therapeutic implications. Cerebrovasc Dis 11:2-8. CrossRef Medline
8. Baron JC, Marchal G (1999) Ischemic core and penumbra in human stroke. Stroke 30:1150-1153. CrossRef Medline
9. Benowitz LI, Carmichael ST (2010) Promoting axonal rewiring to improve outcome after stroke. Neurobiol Dis 37:259-266. CrossRef Medline
10. Blinder P, Tsai PS, Kaufhold JP, Knutsen PM, Suhl H, Kleinfeld D (2013) The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat Neurosci 16:889-897. CrossRef Medline
11. Bolay H, Dalkara T (1998) Mechanisms of motor dysfunction after transient MCA occlusion: persistent transmission failure in cortical synapses is a major determinant. Stroke 29:1988-1993; discussion 1994. CrossRef Medline
12. Bolay H, Gürsoy-Ozdemir Y, Unal I, Dalkara T (2000) Altered mechanisms of motor-evoked potential generation after transient focal cerebral ischemia in the rat: implications for transcranial magnetic stimulation. Brain Res 873:26-33. CrossRef Medline
13. Boyden ES, Zhang F, Bamberg E, Nagel G, DeisserothK (2005) Millisecondtimescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263-1268. CrossRef Medline
14. Buchkremer-Ratzmann I, August M, Hagemann G, WitteOW (1996) Electrophysiological transcortical diaschisis after cortical photothrombosis in rat brain. Stroke 27:1105-1111. CrossRef Medline
15. Bütefisch CM, Netz J, Wessling M, Seitz RJ, Hömberg V (2003) Remote changes in cortical excitability after stroke. Brain 126:470-481. CrossRef Medline
16. Capaday C (2004) The integrated nat of motor cortical function. Neuroscientist 10:207-220. CrossRef Medline
17. Carmichael ST (2012) Brain excitability in stroke: the yin and yang of stroke progression. Arch Neurol 69:161-167. CrossRef Medline
18. Carter AR, Shulman GL, CorbettaM (2012a) Why use a connectivity-based approach to study stroke and recovery of function? Neuroimage 62: 2271-2280. CrossRef Medline
19. Carter AR, Patel KR, Astafiev SV, Snyder AZ, Rengachary J, Strube MJ, Pope A, Shimony JS, Lang CE, Shulman GL, Corbetta M (2012b) Upstream dysfunction of somatomotor functional connectivity after corticospinal damage in stroke. Neurorehabil Neural Repair 26:7-19. CrossRef Medline
20. Castro-Alamancos MA, Borrel J (1995) Functional recovery of forelimb response capacity after forelimb primary motor cortex damage in the rat is due to the reorganization of adjacent areas of cortex. Neuroscience 68: 793-805. CrossRef Medline
21. Cheng H, Luo Q, Wang Z, Gong H, Chen S, Liang W, Zeng S (2003) Efficient characterization of regional mesenteric blood flow by use of laser speckle imaging. Appl Opt 42:5759-5764. CrossRef Medline
22. Chen S, Mohajerani MH, Xie Y, Murphy TH (2012) Optogenetic analysis of neuronal excitability during global ischemia reveals selective deficits in sensory processing following reperfusion in mouse cortex. J Neurosci 32:13510-13519. CrossRef Medline
23. Clarkson AN, Carmichael ST (2009) Cortical excitability and post-stroke recovery. Biochem Soc Trans 37:1412-1414. CrossRef Medline
24. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305-309. CrossRef Medline
25. Cook DJ, Teves L, Tymianski M (2012) Treatment of stroke with a PSD-95 inhibitor in the gyrencephalic primate brain. Nature 483:213-217. CrossRef Medline
26. Cramer SC, Shah R, Juranek J, Crafton KR, Le V (2006) Activity in the peri-infarct rim in relation to recovery from stroke. Stroke 37:111-115. CrossRef Medline
27. Dancause N, Nudo RJ (2011) Shaping plasticity to enhance recovery after injury. Prog Brain Res 192:273-295. CrossRef Medline
28. Devanne H, Lavoie BA, CapadayC (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329-338. Medline
29. Dunn AK, Bolay H, Moskowitz MA, Boas DA (2001) Dynamic imaging of cerebral blood flow using laser speckle. J Cereb Blood Flow Metab 21:195-201. CrossRef Medline
30. Enright LE, Zhang S, Murphy TH (2007) Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J Cereb Blood Flow Metab 27:1185-1200. CrossRef Medline
31. Guggenmos DJ, Azin M, Barbay S, Mahnken JD, Dunham C, Mohseni P, Nudo RJ (2013) Restoration of function after brain damage using a neural prosthesis. Proc Natl Acad Sci U S A 110:21177-21182. CrossRef Medline
32. Harrison TC, Sigler A, Murphy T (2009) Simple and cost-effective hardware and software for functional brain mapping using intrinsic optical signal imaging. J Neurosci Methods 182:211-218. CrossRef Medline
33. Harrison TC, Silasi G, Boyd JD, Murphy TH (2013) Displacement of sensory maps and disorganization of motor cortex after targeted stroke in mice. Stroke 44:2300-2306. CrossRef Medline
34. HeissWD (2000) Ischemic penumbra: evidence from functional imaging in man. J Cereb Blood Flow Metab 20:1276-1293. CrossRef Medline
35. Hershkowitz N, Katchman AN, Veregge S (1993) Site of synaptic depression during hypoxia: a patch-clamp analysis. J Neurophysiol 69:432-441. Medline
36. Hill MD, Martin RH, Mikulis D, Wong JH, Silver FL, Terbrugge KG, Milot G, Clark WM, Macdonald RL, Kelly ME, Boulton M, Fleetwood I, McDougall C, Gunnarsson T, Chow M, Lum C, Dodd R, Poublanc J, Krings T, Demchuk AM, et al. (2012) Safety and efficacy of NA-1 in patients with iatrogenic stroke after endovascular aneurysm repair (ENACT): a phase 2, randomised, double-blind, placebo-controlled trial. Lancet Neurol 11: 942-950. CrossRef Medline
37. Hinman JD, Rasband MN, Carmichael ST (2013) Remodeling of the axon initial segment after focal cortical and white matter stroke. Stroke 44:182-189. CrossRef Medline
38. Hira R, Honkura N, Noguchi J, Maruyama Y, Augustine GJ, Kasai H, MatsuzakiM (2009) Transcranial optogenetic stimulation for functional mapping of the motor cortex. J Neurosci Methods 179:258-263. CrossRef Medline
39. Hofmeijer J, van Putten MJ (2012) Ischemic cerebral damage: an appraisal of synaptic failure. Stroke 43:607-615. CrossRef Medline
40. Horner CH, Davies HA, Stewart MG (1998) Hippocampal synaptic density and glutamate immunoreactivity following transient cerebral ischaemia in the chick. Eur J Neurosci 10:3913-3917. CrossRef Medline
41. Hossmann KA (1971) Cortical steady potential, impedance and excitability changes during and after total ischemia of cat brain. Exp Neurol 32:163-175. CrossRef Medline
42. Hossmann KA (1994) Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557-565. CrossRef Medline
43. Johansen FF, Jørgensen MB, Ekström von Lubitz DK, Diemer NH (1984) Selective dendrite damage in hippocampal CA1 stratum radiatum with unchanged axon ultrastructure and glutamate uptake after transient cerebral ischaemia in the rat. Brain Res 291:373-377. CrossRef Medline
44. Kerr AL, Cheng SY, Jones TA (2011) Experience-dependent neural plasticity in the adult damaged brain. J Commun Disord 44:538-548. CrossRef Medline
45. Khazipov R, Congar P, Ben-Ari Y (1995) Hippocampal CA1 lacunosummoleculare interneurons: comparison of effects of anoxia on excitatory and inhibitory postsynaptic currents. J Neurophysiol 74:2138-2149. Medline
46. Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80:3321-3325. Medline
47. Kleim JA, Barbay S, Cooper NR, Hogg TM, Reidel CN, Remple MS, Nudo RJ (2002) Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem 77:63-77. CrossRef Medline
48. Lashley KS (1931) Mass action in cerebral function. Science 73:245-254. CrossRef Medline
49. Lemon RN (2008) Descending pathways in motor control. Ann Rev Neurosci 31:195-218. CrossRef Medline
50. Levin MF, Kleim JA, Wolf SL (2009) What do motor "recovery" and "compensation" mean in patients following stroke? Neurorehabil Neural Repair 23:313-319. CrossRef Medline
51. Lo EH (2008) A new penumbra: transitioning from injury into repair after stroke. Nat Med 14:497-500. CrossRef Medline
52. Lim DH, Mohajerani MH, Ledue J, Boyd J, Chen S, Murphy TH (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. CrossRef Medline
53. 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:E183-191. CrossRef Medline
54. Moon SK, Alaverdashvili M, Cross AR, Whishaw IQ (2009) Both compensation and recovery of skilled reaching following small photothrombotic stroke to motor cortex in the rat. Exp Neurol 218:145-153. CrossRef Medline
55. Murphy TH (2011) Two-photon imaging of neuronal structual plasticity in mice during and after ischemia. In: Imaging in neuroscience: a laboratory manual, pp. 949-960. New York: Cold Spring Harbor.
56. Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10:861-872. CrossRef Medline
57. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly lightgated cation-selective membrane channel. Proc Natl Acad Sci U S A 100: 13940-13945. CrossRef Medline
58. Nudo RJ (2006) Mechanisms for recovery of motor function following cortical damage. Curr Opin Neurobiol 16:638-644. CrossRef Medline
59. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM (1996a) Usedependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:785-807. Medline
60. Nudo RJ, Wise BM, SiFuentes F, MillikenGW (1996b) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272:1791-1794. CrossRef Medline
61. Nudo RJ, Plautz EJ, Frost SB (2001) Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24:1000-1019. CrossRef Medline
62. Nukada H, Dyck PJ (1987) Acute ischemia causes axonal stasis, swelling, attenuation, and secondary demyelination. Ann Neurol 22:311-318. CrossRef Medline
63. Ohtsubo J, Asakura T (1976) Velocity measurement of a diffuse object by using time-varying speckles. Opt Quant Elect 8:523-529. CrossRef
64. Risher WC, Ard D, Yuan J, Kirov SA (2010) Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci 30:9859-9868. CrossRef Medline
65. Rosen AS, MorrisME (1993) Anoxic depression of excitatory and inhibitory postsynaptic potentials in rat neocortical slices. J Neurophysiol 69:109-117. Medline
66. Schafer DP, Jha S, Liu F, Akella T, McCullough LD, Rasband MN (2009) Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J Neurosci 29:13242-13254. CrossRef Medline
67. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, Kleinfeld D (2006) Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol 4:e22. CrossRef Medline
68. Schmidt S, Bruehl C, Frahm C, Redecker C, Witte OW (2012) Age dependence of excitatory-inhibitory balance following stroke. Neurobiol Aging 33:1356-1363. CrossRef Medline
69. Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Lyden PD, Kleinfeld D (2013) The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci 16:55-63. CrossRef Medline
70. Sigler A, Goroshkov A, Murphy TH (2008) Hardware and methodology for targeting single brain arterioles for photothrombotic stroke on an upright microscope. J Neurosci Methods 170:35-44. CrossRef Medline
71. Sigler A, Mohajerani MH, Murphy TH (2009) Imaging rapid redistribution of sensory-evoked depolarization through existing cortical pathways after targeted stroke in mice. Proc Natl Acad Sci U S A 106:11759-11764. CrossRef Medline
72. Symon L, Branston NM, Strong AJ, Hope TD (1977) The concepts of thresholds of ischaemia in relation to brain structure and function. J Clin Pathol Suppl 11:149-154. Medline
73. 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
74. Tennant KA, Adkins DL, Scalco MD, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA (2012) Skill learning induced plasticity of motor cortical representations is time and age-dependent. Neurobiol Learn Mem 98: 291-302. CrossRef Medline
75. 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. CrossRef Medline
76. Wang JH (2003) Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons in rats. Brain Res Bull 60:53-58. CrossRef Medline
77. 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. CrossRef Medline
78. Xie Y, Chen S, Murphy T (2012) Dendritic spines and pre-synaptic boutons are stable despite local deep hypothermic challenge and re-warming in vivo. PloS one 7:e36305. CrossRef Medline
79. Xie Y, Chen S, Anenberg E, Murphy TH (2013) Resistance of optogenetically evoked motor function to global ischemia and reperfusion in mouse in vivo. J Cereb Blood Flow Metab 33:1148-1152. CrossRef Medline
80. Xiong W, Jin X (2012) Optogenetic field potential recording in cortical slices. J Neurosci Methods 210:119-124. CrossRef Medline
81. Zhang S, Boyd J, Delaney K, Murphy TH (2005) Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J Neurosci 25:5333-5338. CrossRef Medline
82. Zhang S, Murphy TH (2007) Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol 5:e119. CrossRef Medline
83. Zhao G, Flavin MP (2000) Differential sensitivity of rat hippocampal and cortical astrocytes to oxygen-glucose deprivation injury. Neurosci Lett 285:177-180. CrossRef Medline