An optogenetic approach for investigation of excitatory and inhibitory network GABA actions in mice expressing channelrhodopsin-2 in GABAergic neurons

Journal of Neuroscience

Volumn 36, Issue 22, 2016, Pages 5961-5973

  Valeeva, Guzel ^a,b,c   Tressard, Thomas ^a,b   Mukhtarov, Marat ^c   Baude, Agnes ^a,b   Khazipov, Rustem ^a,b,c  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

ChR2; Cortex; GABA; Hippocampus; Inhibition; Interneurons; Optogenetics; Patch clamp

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; RHODOPSIN; TAMOXIFEN; URETHAN; AMINO ACID RECEPTOR AFFECTING AGENT; CHANNELRHODOPSIN 2, MOUSE; GABAERGIC RECEPTOR AFFECTING AGENT; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 2; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN HISTOLOGY; FEMALE; IMMUNOFLUORESCENCE; MALE; MOUSE; NERVE CELL NETWORK; NONHUMAN; OPTOGENETICS; PHOTOACTIVATION; PHOTOSTIMULATION; PRIORITY JOURNAL; AGE; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; NEOCORTEX; NERVE CELL INHIBITION; NEWBORN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; EXCITATORY AMINO ACID AGENTS; GABA AGENTS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; HIPPOCAMPUS; IN VITRO TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, TRANSGENIC; NEOCORTEX; NEURAL INHIBITION; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; RHODOPSIN; SYNAPTIC POTENTIALS;

EID: 84971671571     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3482-15.2016     Document Type: Article

References (70)

1. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22:1042-1053
2. Astorga G, Bao J, Marty A, Augustine GJ, Franconville R, Jalil A, Bradley J, Llano I (2015) An excitatory GABA loop operating in vivo. Front Cell Neurosci 9:275
3. Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159-170
4. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325
5. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215-1284
6. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519
7. Chiu WT, Lin CM, Tsai TC, Wu CW, Tsai CL, Lin SH, Chen JJ (2014) Real-time electrochemical recording of dopamine release under optogenetic stimulation. PLoS One 9:e89293
8. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421
9. Curtis DR, Duggan AW, Felix D, Johnston GA (1970) GABA, bicuculline and central inhibition. Nature 226:1222-1224
10. Dine J, Kuhne C, Deussing JM, Eder M (2014) Optogenetic evocation of field IPSPs in hippocampal slices: a simple and reliable approach for studying pharmacological effects on GABAA and GABAB receptormediated neurotransmission. Front Cell Neurosci 8:2
11. Dzhala V, Valeeva G, Glykys J, Khazipov R, Staley K (2012) Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J Neurosci 32:4017-4031
12. Farrant M, Kaila K (2007) The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 160:59-87
13. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E (2009) Channelrhodopsin-2 is a leaky proton pump. Proc Natl Acad Sci USA 106:12317-12322
14. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470
15. Fu LY, van den Pol AN (2007) GABA excitation in mouse hilar neuropeptide Y neurons. J Physiol 579:445-464
16. Gradmann D, Berndt A, Schneider F, Hegemann P (2011) Rectification of the channelrhodopsin early conductance. Biophys J 101:1057-1068
17. Gulledge AT, Stuart GJ (2003) Excitatory actions of GABA in the cortex. Neuron 37:299-309
18. Han B, Bellemer A, Koelle MR (2015) An evolutionarily conserved switch in response to GABA affects development and behavior of the locomotor circuit of Caenorhabditis elegans. Genetics 199:1159-1172
19. Kätzel D, Zemelman BV, Buetfering C, Wölfel M, Miesenböck G (2011) The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat Neurosci 14:100-107
20. Kaila K, Ruusuvuori E, Seja P, Voipio J, Puskarjov M (2014a) GABA actions and ionic plasticity in epilepsy. Curr Opin Neurobiol 26:34-41
21. Kaila K, Price TJ, Payne JA, Puskarjov M, Voipio J (2014b) Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat Rev Neurosci 15:637-654
22. Katz Y, Yizhar O, Staiger J, Lampl I (2013) Optopatcher-an electrode holder for simultaneous intracellular patch-clamp recording and optical manipulation. J Neurosci Methods 214:113-117
23. Khalilov I, Holmes GL, Ben-Ari Y (2003) In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 6:1079-1085
24. Khalilov I, Minlebaev M, Mukhtarov M, Khazipov R (2015) Dynamic changes from depolarizing to hyperpolarizing GABAergic actions during giant depolarizing potentials in the neonatal rat hippocampus. J Neurosci 35:12635-12642
25. Khazipov R, Valeeva G, Khalilov I (2015) Depolarizing GABA and developmental epilepsies. CNS Neurosci Ther 21:83-91
26. Kirmse K, Witte OW, Holthoff K (2010) GABA depolarizes immature neocortical neurons in the presence of the ketone body -hydroxybutyrate. J Neurosci 30:16002-16007
27. Kirmse K, Kummer M, Kovalchuk Y, Witte OW, Garaschuk O, Holthoff K (2015) GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo. Nat Commun 6:7750
28. Krnjevic K, Phillis JW (1963) Iontophoretic studies of neurones in the mammalian cerebral cortex. J Physiol 165:274-304
29. Ladas TP, Chiang CC, Gonzalez-Reyes LE, Nowak T, Durand DM (2015) Seizure reduction through interneuron-mediated entrainment using low frequency optical stimulation. Exp Neurol 269:120-132
30. Ledri M, Madsen MG, Nikitidou L, Kirik D, Kokaia M (2014) Global optogenetic activation of inhibitory interneurons during epileptiform activity. J Neurosci 34:3364-3377
31. 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
32. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH, Nicoud JF, Zemelman BV, Sternson SM, Losonczy A (2012) Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15: 423-430, S1-S3
33. Luna VM, Morozov A (2012) Input-specific excitation of olfactory cortex microcircuits. Front Neural Circuits 6:69
34. Marissal T, Bonifazi P, Picardo MA, Nardou R, Petit LF, Baude A, Fishell GJ, Ben-Ari Y, Cossart R (2012) Pioneer glutamatergic cells develop into a morpho-functionally distinct population in the juvenile CA3 hippocampus. Nat Commun 3:1316
35. Mazzuca M, Minlebaev M, Shakirzyanova A, Tyzio R, Taccola G, Janackova S, Gataullina S, Ben-Ari Y, Giniatullin R, Khazipov R (2011) Newborn analgesia mediated by oxytocin during delivery. Front Cell Neurosci 5:3
36. Mercer LF Jr, Remley NR, Gilman DP (1978) Effects of urethane on hippocampal unit activity in the rat. Brain Res Bull 3:567-570.
37. Minlebaev M, Ben-Ari Y, Khazipov R (2007) Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 97:692-700
38. Minlebaev M, Valeeva G, Tcheremiskine V, Coustillier G, Khazipov R (2013) Cell-attached recordings of responses evoked by photorelease of GABA in the immature cortical neurons. Front Cell Neurosci 7:83
39. Mitrukhina O, Suchkov D, Khazipov R, Minlebaev M (2015) Imprecise whisker map in the neonatal rat barrel cortex. Cereb Cortex 25:3458-3467
40. Mody I, Heinemann U (1986) Laminar profiles of the changes in extracellular calcium concentration induced by repetitive stimulation and excitatory amino acids in the rat dentate gyrus. Neurosci Lett 69:137-142
41. Moore AK, Wehr M (2013) Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci 33: 13713-13723
42. Nabekura J, Ueno T, Okabe A, Furuta A, Iwaki T, Shimizu-Okabe C, Fukuda A, Akaike N (2002) Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury. J Neurosci 22: 4412-4417
43. Nagel G, Szellas T, Kateriya S, Huhn W, 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
44. Nicholson C, Steinberg R, Stöckle H, Bruggencate GT (1976) Calcium decrease associated with aminopyridine-induced potassium increase in cat cerebellum. Neurosci Lett 3:315-319
45. Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW (2013) Oxytocin enhances hippocampal spike transmission by modulating fastspiking interneurons. Nature 500:458-462
46. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727
47. Owens DF, Liu X, Kriegstein AR (1999) Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J Neurophysiol 82:570-583
48. 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
49. Price TJ, Cervero F, Gold MS, Hammond DL, Prescott SA (2009) Chloride regulation in the pain pathway. Brain Res Rev 60:149-170
50. Quattrocolo G, Maccaferri G (2013) Novel GABAergic circuits mediating excitation/inhibition of Cajal-Retzius cells in the developing hippocampus. J Neurosci 33:5486-5498
51. Rheims S, Holmgren CD, Chazal G, Mulder J, Harkany T, Zilberter T, Zilberter Y (2009) GABA action in immature neocortical neurons directly depends on the availability of ketone bodies. J Neurochem 110:1330-1338
52. Rivera C, Voipio J, Kaila K (2005) Two developmental switches in GABAergic signalling: the K -Cl cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562:27-36
53. Romo-Parra H, Treviño M, Heinemann U, Gutiérrez R (2008) GABA actions in hippocampal area CA3 during postnatal development: differential shift from depolarizing to hyperpolarizing in somatic and dendritic compartments. J Neurophysiol 99:1523-1534
54. Ruusuvuori E, Kirilkin I, Pandya N, Kaila K (2010) Spontaneous network events driven by depolarizing GABA action in neonatal hippocampal slices are not attributable to deficient mitochondrial energy metabolism. J Neurosci 30:15638-15642
55. Sachidhanandam S, Sreenivasan V, Kyriakatos A, Kremer Y, Petersen CC (2013) Membrane potential correlates of sensory perception in mouse barrel cortex. Nat Neurosci 16:1671-1677
56. Sceniak MP, MacIver B (2006) Cellular actions of urethane on rat visual cortical neurons in vitro. J Neurophysiol 95:3865-3874.
57. Schlingloff D, Káli S, Freund TF, Hájos N, Gulyás A (2014) Mechanisms of sharp wave initiation and ripple generation. J Neurosci 34:11385-11398
58. Stark E, Eichler R, Roux L, Fujisawa S, Rotstein HG, Buzsáki G (2013) Inhibition-induced theta resonance in cortical circuits. Neuron 80: 1263-1276
59. Szabadics J, Varga C, Molnár G, Oláh S, Barzó P, Tamás G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233-235
60. Szydlowski SN, Pollak Dorocic I, Planert H, Carlén M, Meletis K, Silberberg G (2013) Target selectivity of feedforward inhibition by striatal fast-spiking interneurons. J Neurosci 33:1678-1683
61. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314: 1788-1792
62. Tyzio R, Holmes GL, Ben-Ari Y, Khazipov R (2007) Timing of the developmental switch in GABA(A)-mediated signalling from excitation to inhibition in CA3 rat hippocampus using gramicidin perforated patch and extracellular recordings. Epilepsia 48:96-105
63. Tyzio R, Minlebaev M, Rheims S, Ivanov A, Jorquera I, Holmes GL, Zilberter Y, Ben-Ari Y, Khazipov R (2008) Postnatal changes in somatic gammaaminobutyric acid signalling in the rat hippocampus. Eur J Neurosci 27: 2515-2528
64. Tyzio R, Allene C, Nardou R, Picardo MA, Yamamoto S, Sivakumaran S, Caiati MD, Rheims S, Minlebaev M, Milh M, Ferré P, Khazipov R, Romette JL, Lorquin J, Cossart R, Khalilov I, Nehlig A, Cherubini E, Ben-Ari Y (2011) Depolarizing actions of GABA in immature neurons depend neither on ketone bodies nor on pyruvate. J Neurosci 31:34-45
65. Valeeva G, Valiullina F, Khazipov R (2013) Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front Cell Neurosci 7:20
66. van den Pol AN, Obrietan K, Chen G (1996) Excitatory actions of GABA after neuronal trauma. J Neurosci 16:4283-4292
67. Wang H, Sugiyama Y, Hikima T, Sugano E, Tomita H, Takahashi T, Ishizuka T, Yawo H (2009) Molecular determinants differentiating photocurrent properties of two channelrhodopsins from Chlamydomonas. J Biol Chem 284:5685-5696
68. Willis WD (2006) John Eccles’ studies of spinal cord presynaptic inhibition. Prog Neurobiol 78:189-214
69. Windmuller O, Lindauer U, Foddis M, Einhäupl KM, Dirnagl U, Heinemann U, Dreier JP (2005) Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 128:2042-2051
70. Woodruff AR, McGarry LM, Vogels TP, Inan M, Anderson SA, Yuste R (2011) State-dependent function of neocortical chandelier cells. J Neurosci 31:17872-17886