Astrocytes regulate cortical state switching in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 19, 2016, Pages E2675-E2684

  Poskanzer, Kira E ^a,b   Yuste, Rafael ^a  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; Calcium imaging; Cortex; Glutamate; Slow oscillation

Indexed keywords

CALCIUM; GLUTAMIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGICAL ASSAY; EXTRACELLULAR SPACE; IN VIVO STUDY; MEMORY; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; OPTOGENETICS; OSCILLATION; PRIORITY JOURNAL; SLEEP; ANIMAL; BIOLOGICAL RHYTHM; BRAIN MAPPING; C57BL MOUSE; CALCIUM SIGNALING; CELL COMMUNICATION; CELL CULTURE; FEMALE; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BIOLOGICAL CLOCKS; BRAIN MAPPING; CALCIUM; CALCIUM SIGNALING; CELL COMMUNICATION; CELLS, CULTURED; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOCORTEX; NEURONS; SYNAPTIC TRANSMISSION;

EID: 84966356663     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1520759113     Document Type: Article

References (82)

1. Steriade M, Nuñez A, Amzica F (1993) A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. J Neurosci 13(8):3252-3265.
2. Hughes SW, Cope DW, Blethyn KL, Crunelli V (2002) Cellular mechanisms of the slow (<1 Hz) oscillation in thalamocortical neurons in vitro. Neuron 33(6):947-958.
3. Isomura Y, et al. (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52(5):871-882.
4. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10(1):100-107.
5. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: A view from inside neocortical neurons. J Neurophysiol 85(5):1969-1985.
6. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100(23):13638-13643.
7. Okun M, Naim A, Lampl I (2010) The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J Neurosci 30(12):4440-4448.
8. Luczak A, Barthó P, Harris KD (2009) Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62(3):413-425.
9. Nir Y, et al. (2011) Regional slow waves and spindles in human sleep. Neuron 70(1):153-169.
10. Vyazovskiy VV, et al. (2011) Local sleep in awake rats. Nature 472(7344):443-447.
11. Steriade M, Nuñez A, Amzica F (1993) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13(8):3266-3283.
12. Amzica F, Steriade M (1995) Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J Neurosci 15(6):4658-4677.
13. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10(12):1185-1199.
14. Cossart R, Aronov D, Yuste R (2003) Attractor dynamics of network UP states in the neocortex. Nature 423(6937):283-288.
15. Zagha E, Casale AE, Sachdev RN, McGinley MJ, McCormick DA (2013) Motor cortex feedback influences sensory processing by modulating network state. Neuron 79(3):567-578.
16. Pinto L, et al. (2013) Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16(12):1857-1863.
17. Bermudez Contreras EJ, et al. (2013) Formation and reverberation of sequential neural activity patterns evoked by sensory stimulation are enhanced during cortical desynchronization. Neuron 79(3):555-566.
18. Poulet JF, Fernandez LM, Crochet S, Petersen CC (2012) Thalamic control of cortical states. Nat Neurosci 15(3):370-372.
19. Reimer J, et al. (2014) Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 84(2):355-362.
20. Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci USA 108(45):18453-18458.
21. Halassa MM, et al. (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61(2):213-219.
22. Fellin T, et al. (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci USA 106(35):15037-15042.
23. Wang F, Xu Q, Wang W, Takano T, Nedergaard M (2012) Bergmann glia modulate cerebellar Purkinje cell bistability via Ca2+ -dependent K+ uptake. Proc Natl Acad Sci USA 109(20):7911-7916.
24. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22(1):183-192.
25. Fujita T, et al. (2014) Neuronal transgene expression in dominant-negative SNARE mice. J Neurosci 34(50):16594-16604.
26. Sloan SA, Barres BA (2014) Looks can be deceiving: Reconsidering the evidence for gliotransmission. Neuron 84(6):1112-1115.
27. Lee HS, et al. (2014) Astrocytes contribute to gamma oscillations and recognition memory. Proc Natl Acad Sci USA 111(32):E3343-E3352.
28. Ding F, et al. (2013) α1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice. Cell Calcium 54(6):387-394.
29. Paukert M, et al. (2014) Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82(6):1263-1270.
30. Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS (2011) TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat Neurosci 15(1):70-80.
31. Chen TW, et al. (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295-300.
32. Kanemaru K, et al. (2014) In vivo visualization of subtle, transient, and local activity of astrocytes using an ultrasensitive Ca(2+) indicator. Cell Reports 8(1):311-318.
33. Haustein MD, et al. (2014) Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway. Neuron 82(2):413-429.
34. Di Castro MA, et al. (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14(10):1276-1284.
35. Otsu Y, et al. (2015) Calcium dynamics in astrocyte processes during neurovascular coupling. Nat Neurosci 18(2):210-218.
36. Reeves AM, Shigetomi E, Khakh BS (2011) Bulk loading of calcium indicator dyes to study astrocyte physiology: Key limitations and improvements using morphological maps. J Neurosci 31(25):9353-9358.
37. Hirase H, Qian L, Barthó P, Buzsáki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2(4):E96.
38. Bonder DE, McCarthy KD (2014) Astrocytic Gq-GPCR-linked IP3R-dependent Ca2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo. J Neurosci 34(39):13139-13150.
39. Ortinski PI, et al. (2010) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13(5):584-591.
40. Shigetomi E, et al. (2013) Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141(5):633-647.
41. Pagliardini S, Gosgnach S, Dickson CT (2013) Spontaneous sleep-like brain state alternations and breathing characteristics in urethane anesthetized mice. PLoS One 8(7):e70411.
42. Murakami M, Kashiwadani H, Kirino Y, Mori K (2005) State-dependent sensory gating in olfactory cortex. Neuron 46(2):285-296.
43. Mishima T, Hirase H (2010) In vivo intracellular recording suggests that gray matter astrocytes in mature cerebral cortex and hippocampus are electrophysiologically homogeneous. J Neurosci 30(8):3093-3100.
44. Gervasoni D, et al. (2004) Global forebrain dynamics predict rat behavioral states and their transitions. J Neurosci 24(49):11137-11147.
45. Chow BY, et al. (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463(7277):98-102.
46. Takano T, et al. (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9(2):260-267.
47. Panatier A, et al. (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146(5):785-798.
48. Gourine AV, et al. (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329(5991):571-575.
49. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324(5925):354-359.
50. Agulhon C, Fiacco TA, McCarthy KD (2010) Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 327(5970):1250-1254.
51. Perea G, Yang A, Boyden ES, Sur M (2014) Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat Commun 5:3262.
52. McKhann GM, II, D'Ambrosio R, Janigro D (1997) Heterogeneity of astrocyte resting membrane potentials and intercellular coupling revealed by whole-cell and gramicidin-perforated patch recordings from cultured neocortical and hippocampal slice astrocytes. J Neurosci 17(18):6850-6863.
53. Tang F, et al. (2014) Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5:3284.
54. Beppu K, et al. (2014) Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage. Neuron 81(2):314-320.
55. Volgushev M, Chauvette S, Mukovski M, Timofeev I (2006) Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations [corrected]. J Neurosci 26(21):5665-5672.
56. Lind BL, Brazhe AR, Jessen SB, Tan FC, Lauritzen MJ (2013) Rapid stimulus-evoked astrocyte Ca2+ elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc Natl Acad Sci USA 110(48):E4678-E4687.
57. Nizar K, et al. (2013) In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J Neurosci 33(19):8411-8422.
58. Gonçalves JT, Anstey JE, Golshani P, Portera-Cailliau C (2013) Circuit level defects in the developing neocortex of Fragile X mice. Nat Neurosci 16(7):903-909.
59. Marvin JS, et al. (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods 10(2):162-170.
60. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3(10):1027-1034.
61. Parpura V, Verkhratsky A (2012) Astrocytes revisited: Concise historic outlook on glutamate homeostasis and signaling. Croat Med J 53(6):518-528.
62. Hirase H, Iwai Y, Takata N, Shinohara Y, Mishima T (2014) Volume transmission signalling via astrocytes. Philos Trans R Soc Lond B Biol Sci 369(1654):20130604.
63. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16(16):5073-5081.
64. Fiacco TA, McCarthy KD (2006) Astrocyte calcium elevations: Properties, propagation, and effects on brain signaling. Glia 54(7):676-690.
65. Quirin S, Peterka DS, Yuste R (2013) Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging. Opt Express 21(13):16007-16021.
66. Cheng A, Gonçalves JT, Golshani P, Arisaka K, Portera-Cailliau C (2011) Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing. Nat Methods 8(2):139-142.
67. Chia TH, Levene MJ (2009) Microprisms for in vivo multilayer cortical imaging. J Neurophysiol 102(2):1310-1314.
68. Abrahamsson S, et al. (2013) Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat Methods 10(1):60-63.
69. Beltramo R, et al. (2013) Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat Neurosci 16(2):227-234.
70. Bellesi M, de Vivo L, Tononi G, Cirelli C (2015) Effects of sleep and wake on astrocytes: Clues from molecular and ultrastructural studies. BMC Biol 13:66
71. Pannasch U, et al. (2014) Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 17(4):549-558.
72. Bernardinelli Y, et al. (2014) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Curr Biol 24(15):1679-1688.
73. Constantinople CM, Bruno RM (2011) Effects and mechanisms of wakefulness on local cortical networks. Neuron 69(6):1061-1068.
74. Niell CM, Stryker MP (2010) Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65(4):472-479.
75. Polack PO, Friedman J, Golshani P (2013) Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat Neurosci 16(9):1331-1339.
76. Bennett C, Arroyo S, Hestrin S (2013) Subthreshold mechanisms underlying statedependent modulation of visual responses. Neuron 80(2):350-357.
77. Lee SH, Dan Y (2012) Neuromodulation of brain states. Neuron 76(1):209-222.
78. Zhuang J, et al. (2014) Brain state effects on layer 4 of the awake visual cortex. J Neurosci 34(11):3888-3900.
79. Fu Y, et al. (2014) A cortical circuit for gain control by behavioral state. Cell 156(6):1139-1152.
80. Froudarakis E, et al. (2014) Population code in mouse V1 facilitates readout of natural scenes through increased sparseness. Nat Neurosci 17(6):851-857.
81. Nikolenko V, Poskanzer KE, Yuste R (2007) Two-photon photostimulation and imaging of neural circuits. Nat Methods 4(11):943-950.
82. Vogelstein JT, et al. (2010) Fast nonnegative deconvolution for spike train inference from population calcium imaging. J Neurophysiol 104(6):3691-3704.