Prolonged deficits in parvalbumin neuron stimulation-evoked network activity despite recovery of dendritic structure and excitability in the somatosensory cortex following global ischemia in mice

Journal of Neuroscience

Volumn 34, Issue 45, 2014, Pages 14890-14900

  Xie, Yicheng ^a,b   Chen, Shangbin ^a,b   Wu, Yujin ^a,b   Murphy, Timothy H ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Inhibitory synaptic transmission; Optogenetics; Parvalbumin neuron; Reperfusion; Stroke; Two photon imaging

Indexed keywords

PARVALBUMIN; 4 AMINOBUTYRIC ACID RECEPTOR; CHANNELRHODOPSIN 2, MOUSE; RHODOPSIN;

ACTION POTENTIAL; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; ELECTROENCEPHALOGRAPHY; EVOKED SOMATOSENSORY RESPONSE; FUNCTIONAL ASSESSMENT; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNAL CAROTID ARTERY OCCLUSION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE CONDUCTION DISORDER; NERVE EXCITABILITY; NERVE STIMULATION; NONHUMAN; OPTOGENETICS; PATCH CLAMP TECHNIQUE; PROTEIN EXPRESSION; SIGNAL NOISE RATIO; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN INFARCTION; C57BL MOUSE; DENDRITE; GENETICS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CEREBRAL INFARCTION; DENDRITES; GABAERGIC NEURONS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MICE; MICE, INBRED C57BL; OPTOGENETICS; PARVALBUMINS; RHODOPSIN; SOMATOSENSORY CORTEX;

EID: 84908518650     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1775-14.2014     Document Type: Article

References (79)

1. Alicke B, Schwartz-Bloom RD (1995) Rapid down-regulation of GABA(A) receptors in the gerbil hippocampus following transient cerebral ischemia. J Neurochem 65:2808-2811. CrossRef Medline
2. Allen NJ, Rossi DJ, Attwell D (2004) Sequential release of GABA by exocytosis and reversed uptake leads to neuronal swelling in simulated ischemia of hippocampal slices. J Neurosci 24:3837-3849. CrossRef Medline
3. Anderson TR, Jarvis CR, Biedermann AJ, Molnar C, Andrew RD (2005) Blocking the anoxic depolarization protects without functional compromise following simulated stroke in cortical brain slices. J Neurophysiol 93:963-979.Medline
4. Andrew RD, Labron MW, Boehnke SE, Carnduff L, Kirov SA (2007) Physiological evidence that pyramidal neurons lack functional water channels. Cereb Cortex 17:787-802. CrossRef Medline
5. Block F (1999) Global ischemia and behavioural deficits. Prog Neurobiol 58:279-295. CrossRef Medline
6. 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. CrossRef Medline
7. Buchkremer-Ratzmann I, Witte OW (1997) Extended brain disinhibition following small photothrombotic lesions in rat frontal cortex. Neuroreport 8:519-522. CrossRef Medline
8. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667. CrossRef Medline
9. Carmichael ST (2012) Brain excitability in stroke: the yin and yang of stroke progression. Arch Neurol 69:161-167. CrossRef Medline
10. Chavez JC, LaManna JC (2002) Activation of hypoxia-inducible factor-1 in the rat cerebral cortex after transient global ischemia: potential role of insulin-like growth factor-1. J Neurosci 22:8922-8931.Medline
11. Chen Q, Cichon J, Wang W, Qiu L, Lee SJ, Campbell NR, Destefino N, Goard MJ, Fu Z, Yasuda R, Looger LL, Arenkiel BR, Gan WB, Feng G (2012) Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76: 297-308. CrossRef Medline
12. Chen S, Tran S, Sigler A, Murphy TH (2011) Automated and quantitative image analysis of ischemic dendritic blebbing using in vivo 2-photon microscopy data. J Neurosci Methods 195:222-231. CrossRef Medline
13. 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
14. Chen Z, Xiong C, Pancyr C, Stockwell J, Walz W, Cayabyab FS (2014) Prolonged adenosine A1 receptor activation in hypoxia and pial vessel disruption focal cortical ischemia facilitates clathrin-mediated AMPA receptor endocytosis and long-lasting synaptic inhibition in rat hippocampal CA3-CA1 synapses: differential regulation of GluA2 and GluA1 subunits by p38 MAPK and JNK. J Neurosci 34:9621-9643. CrossRef Medline
15. Cheng MY, Wang EH, Woodson WJ, Wang S, Sun G, Lee AG, Arac A, Fenno LE, Deisseroth K, Steinberg GK (2014) Optogenetic neuronal stimulation promotes functional recovery after stroke. Proc Natl Acad Sci U S A 111:12913-12918. CrossRef Medline
16. 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
17. Clarkson AN, Overman JJ, Zhong S, Mueller R, Lynch G, Carmichael ST (2011) AMPA receptor-induced local brain-derived neurotrophic factor signaling mediates motor recovery after stroke. J Neurosci 31:3766-3775. CrossRef Medline
18. Constantinople CM, Bruno RM (2011) Effects and mechanisms of wakefulness on local cortical networks. Neuron 69:1061-1068. CrossRef Medline
19. Drew PJ, Shih AY, Driscoll JD, Knutsen PM, Blinder P, Davalos D, Akassoglou K, Tsai PS, Kleinfeld D (2010) Chronic optical access through a polished and reinforced thinned skull. Nat Methods 7:981-984. CrossRef Medline
20. Freund TF, Buzsáki G, Leon A, Baimbridge KG, Somogyi P (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp Brain Res 83:55-66. CrossRef Medline
21. Fujii M, Hara H, Meng W, Vonsattel JP, Huang Z, Moskowitz MA (1997) Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 28:1805-1810; discussion 1811. CrossRef Medline
22. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, Diester I, Goshen I, Thompson KR, Deisseroth K (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:154-165. CrossRef Medline
23. Harrison TC, Ayling OG, Murphy TH (2012) Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography. Neuron 74:397-409. CrossRef Medline
24. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hübener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L (2009) Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4:1128-1144. CrossRef Medline
25. 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
26. Hossmann KA, Sato K (1970) Recovery of neuronal function after prolonged cerebral ischemia. Science 168:375-376. CrossRef Medline
27. Hummel FC, Cohen LG (2006) Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5:708-712. CrossRef Medline
28. Ilie A, Ciocan D, Zagrean AM, Nita DA, Zagrean L, Moldovan M (2006) Endogenous activation of adenosine A(1) receptors accelerates ischemic suppression of spontaneous electrocortical activity. J Neurophysiol 96: 2809-2814. CrossRef Medline
29. Jarvis CR, Anderson TR, Andrew RD (2001) Anoxic depolarization mediates acute damage independent of glutamate in neocortical brain slices. Cereb Cortex 11:249-259. CrossRef Medline
30. Johansen FF, Tønder N, Zimmer J, Baimbridge KG, Diemer NH (1990) Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci Lett 120:171-174. CrossRef Medline
31. Kahn I, Desai M, Knoblich U, Bernstein J, Henninger M, Graybiel AM, Boyden ES, Buckner RL, Moore CI (2011) Characterization of the functional MRI response temporal linearity via optical control of neocortical pyramidal neurons. J Neurosci 31:15086-15091. CrossRef Medline
32. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, Morimoto TK, Chuong AS, Carpenter EJ, Tian Z, Wang J, Xie Y, Yan Z, Zhang Y, Chow BY, Surek B, Melkonian M, Jayaraman V, Constantine-Paton M, Wong GK, et al. (2014) Independent optical excitation of distinct neural populations. Nat Methods 11:338-346. CrossRef Medline
33. Koh JY, Suh SW, Gwag BJ, He YY, Hsu CY, Choi DW (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016. CrossRef Medline
34. Krakauer JW, Carmichael ST, Corbett D, Wittenberg GF (2012) Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair 26:923-931. CrossRef Medline
35. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622-626. CrossRef Medline
36. Kuhlman SJ, Huang ZJ (2008) High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLoS One 3:e2005. CrossRef Medline
37. Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES, Deisseroth K, Dan Y (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379-383. CrossRef Medline
38. Lesnick JE, Michele JJ, Simeone FA, DeFeo S, Welsh FA (1984) Alteration of somatosensory evoked potentials in response to global ischemia. J Neurosurg 60:490-494. CrossRef Medline
39. Lim C, Alexander MP, LaFleche G, Schnyer DM, Verfaellie M (2004) The neurological and cognitive sequelae of cardiac arrest. Neurology 63: 1774-1778. CrossRef Medline
40. Lin JY, Knutsen PM, Muller A, Kleinfeld D, Tsien RY (2013) ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat Neurosci 16:1499-1508. CrossRef Medline
41. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140. CrossRef Medline
42. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807. CrossRef Medline
43. McKhann GM, Borowicz LM, Goldsborough MA, Enger C, Selnes OA (1997) Depression and cognitive decline after coronary artery bypass grafting. Lancet 349:1282-1284. CrossRef Medline
44. Mégevand P, Troncoso E, Quairiaux C, Muller D, Michel CM, Kiss JZ (2009) Long-term plasticity in mouse sensorimotor circuits after rhythmic whisker stimulation. J Neurosci 29:5326-5335. CrossRef Medline
45. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37-100.Medline
46. 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. CrossRef Medline
47. 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. CrossRef Medline
48. Murphy TH, Li P, Betts K, Liu R (2008) Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci 28:1756-1772. CrossRef Medline
49. Nitsch C, Scotti A, Sommacal A, Kalt G (1989) GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2(+)-binding protein parvalbumin. Neurosci Lett 105:263-268. CrossRef Medline
50. Nunn J, Hodges H (1994) Cognitive deficits induced by global cerebral ischaemia: relationship to brain damage and reversal by transplants. Behav Brain Res 65:1-31. CrossRef Medline
51. Panahian N, Yoshida T, Huang PL, Hedley-Whyte ET, Dalkara T, Fishman MC, Moskowitz MA (1996) Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience 72:343-354. CrossRef Medline
52. Pang ZP, Deng P, Ruan YW, Xu ZC (2002) Depression of fast excitatory synaptic transmission in large aspiny neurons of the neostriatum after transient forebrain ischemia. J Neurosci 22:10948-10957.Medline
53. Petersen CC, Hahn TTG, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A 100:13638-13643. CrossRef Medline
54. Pettersen KH, Devor A, Ulbert I, Dale AM, Einevoll GT (2006) Currentsource density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities. J Neurosci Methods 154:116-133. CrossRef Medline
55. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068-1076. CrossRef Medline
56. Qü M, Mittmann T, Luhmann HJ, Schleicher A, Zilles K (1998) Long-term changes of ionotropic glutamate and GABA receptors after unilateral permanent focal cerebral ischemia in the mouse brain. Neuroscience 85:29-43. CrossRef Medline
57. Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661-1687. CrossRef Medline
58. Ren JQ, Aika Y, Heizmann CW, Kosaka T (1992) Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp Brain Res 92:1-14. CrossRef Medline
59. 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
60. Risher WC, Croom D, Kirov SA (2012) Persistent astroglial swelling accompanies rapid reversible dendritic injury during stroke-induced spreading depolarizations. Glia 60:1709-1720. CrossRef Medline
61. Runyan CA, Schummers J, Van Wart A, Kuhlman SJ, Wilson NR, Huang ZJ, Sur M (2010) Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 67:847-857. CrossRef Medline
62. Sheng H, Laskowitz DT, Pearlstein RD, Warner DS (1999) Characterization of a recovery global cerebral ischemia model in the mouse. J Neurosci Methods 88:103-109. CrossRef Medline
63. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762. CrossRef Medline
64. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995-1013. CrossRef Medline
65. Thompson RJ, Zhou N, MacVicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science 312:924-927. CrossRef Medline
66. Torrey EF, Barci BM, Webster MJ, Bartko JJ, Meador-Woodruff JH, Knable MB (2005) Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol Psychiatry 57:252-260. CrossRef Medline
67. Tortosa A, Ferrer I (1993) Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischaemia: a qualitative and quantitative sequential study. Neuroscience 55:33-43. CrossRef Medline
68. Tran S, Chen S, Liu RR, Xie Y, Murphy TH (2012) Moderate or deep local hypothermia does not prevent the onset of ischemia-induced dendritic damage. J Cereb Blood Flow Metab 32:437-442. CrossRef Medline
69. Tye KM, Deisseroth K (2012) Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13:251-266. CrossRef Medline
70. 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
71. Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343-348. CrossRef Medline
72. Xie Y, Wang T, Sun GY, Ding S (2010) Specific disruption of astrocytic Ca2_ signaling pathway in vivo by adeno-associated viral transduction. Neuroscience 170:992-1003. CrossRef Medline
73. 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
74. 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
75. Yang G, Pan F, Parkhurst CN, Grutzendler J, Gan WB (2010) Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat Protoc 5:201-208. CrossRef Medline
76. Zhan RZ, Nadler JV, Schwartz-Bloom RD (2006) Depressed responses to applied and synaptically-released GABA in CA1 pyramidal cells, but not in CA1 interneurons, after transient forebrain ischemia. J Cereb Blood Flow Metab 26:112-124. CrossRef Medline
77. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, de Lecea L, Deisseroth K (2010) Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5:439-456. CrossRef Medline
78. 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
79. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.Medline