1932

Abstract

Animal behavior was classically considered to be determined exclusively by neuronal activity, whereas surrounding glial cells such as astrocytes played only supportive roles. However, astrocytes are as numerous as neurons in the mammalian brain, and current findings indicate a chemically based dialog between astrocytes and neurons. Activation of astrocytes by synaptically released neurotransmitters converges on regulating intracellular Ca2+ in astrocytes, which then can regulate the efficacy of near and distant tripartite synapses at diverse timescales through gliotransmitter release. Here, we discuss recent evidence on how diverse behaviors are impacted by this dialog. These recent findings support a paradigm shift in neuroscience, in which animal behavior does not result exclusively from neuronal activity but from the coordinated activity of both astrocytes and neurons. Decoding how astrocytes and neurons interact with each other in various brain circuits will be fundamental to fully understanding how behaviors originate and become dysregulated in disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-101920-112225
2021-07-08
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/neuro/44/1/annurev-neuro-101920-112225.html?itemId=/content/journals/10.1146/annurev-neuro-101920-112225&mimeType=html&fmt=ahah

Literature Cited

  1. Adamsky A, Goshen I. 2018. Astrocytes in memory function: pioneering findings and future directions. Neuroscience 370:14–26
    [Google Scholar]
  2. Adamsky A, Kol A, Kreisel T, Doron A, Ozeri-Engelhard N et al. 2018. Astrocytic activation generates de novo neuronal potentiation and memory enhancement. Cell 174:59–71.e14
    [Google Scholar]
  3. Andersen JD, Pouzet B. 2004. Spatial memory deficits induced by perinatal treatment of rats with PCP and reversal effect of d-serine. Neuropsychopharmacology 29:1080–90
    [Google Scholar]
  4. Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A. 2014. Gliotransmitters travel in time and space. Neuron 81:728–39
    [Google Scholar]
  5. Arrigoni E, Chee MJS, Fuller PM. 2019. To eat or to sleep: That is a lateral hypothalamic question. Neuropharmacology 154:34–49
    [Google Scholar]
  6. Bado P, Madeira C, Vargas-Lopes C, Moulin TC, Wasilewska-Sampaio AP et al. 2011. Effects of low-dose d-serine on recognition and working memory in mice. Psychopharmacology 218:461–70
    [Google Scholar]
  7. Balleine BW. 2007. The neural basis of choice and decision making. J. Neurosci. 27:8159–60
    [Google Scholar]
  8. Banasr M, Duman RS. 2008. Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol. Psychiatry 64:863–70
    [Google Scholar]
  9. Barca-Mayo O, Boender AJ, Armirotti A, De Pietri, Tonelli D. 2020. Deletion of astrocytic BMAL1 results in metabolic imbalance and shorter lifespan in mice. Glia 68:1131–47
    [Google Scholar]
  10. Barros LF, Weber B. 2018. CrossTalk proposal: an important astrocyte-to-neuron lactate shuttle couples neuronal activity to glucose utilisation in the brain. J. Physiol. 596:347–50
    [Google Scholar]
  11. Benneyworth MA, Li Y, Basu AC, Bolshakov VY, Coyle JT. 2012. Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons. Cell Mol. Neurobiol. 32:613–24
    [Google Scholar]
  12. Bjorness TE, Dale N, Mettlach G, Sonneborn A, Sahin B et al. 2016. An adenosine-mediated glial-neuronal circuit for homeostatic sleep. J. Neurosci. 36:3709–21
    [Google Scholar]
  13. Boury-Jamot B, Carrard A, Martin JL, Halfon O, Magistretti PJ, Boutrel B. 2016. Disrupting astrocyte–neuron lactate transfer persistently reduces conditioned responses to cocaine. Mol. Psychiatry 21:1070–76
    [Google Scholar]
  14. Brancaccio M, Patton AP, Chesham JE, Maywood ES, Hastings MH. 2017. Astrocytes control circadian timekeeping in the suprachiasmatic nucleus via glutamatergic signaling. Neuron 93:1420–35.e5
    [Google Scholar]
  15. Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S et al. 2010. Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J. Neurosci. 30:4590–600
    [Google Scholar]
  16. Brown AM, Baltan Tekkök S, Ransom BR. 2004. Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem. Int. 45:529–36
    [Google Scholar]
  17. Cai W, Xue C, Sakaguchi M, Konishi M, Shirazian A et al. 2018. Insulin regulates astrocyte gliotransmission and modulates behavior. J. Clin. Investig. 128:2914–26
    [Google Scholar]
  18. Calì C, Tauffenberger A, Magistretti P. 2019. The strategic location of glycogen and lactate: from body energy reserve to brain plasticity. Front. Cell. Neurosci. 13:82
    [Google Scholar]
  19. Cao B, Wang J, Mu L, Poon DC-H, Li Y. 2016. Impairment of decision making associated with disruption of phase-locking in the anterior cingulate cortex in viscerally hypersensitive rats. Exp. Neurol. 286:21–31
    [Google Scholar]
  20. Cao X, Li L-P, Wang Q, Wu Q, Hu H-H et al. 2013. Astrocyte-derived ATP modulates depressive-like behaviors. Nat. Med. 19:773–77
    [Google Scholar]
  21. Carson MJ, Thomas EA, Danielson PE, Sutcliffe JG. 1996. The 5HT5A serotonin receptor is expressed predominantly by astrocytes in which it inhibits cAMP accumulation: a mechanism for neuronal suppression of reactive astrocytes. Glia 17:317–26
    [Google Scholar]
  22. Chen J, Tan Z, Zeng L, Zhang X, He Y et al. 2013. Heterosynaptic long-term depression mediated by ATP released from astrocytes. Glia 61:178–91
    [Google Scholar]
  23. Chen N, Sugihara H, Kim J, Fu Z, Barak B et al. 2016. Direct modulation of GFAP-expressing glia in the arcuate nucleus bi-directionally regulates feeding. eLife 5:e18716
    [Google Scholar]
  24. Chen N, Sugihara H, Sharma J, Perea G, Petravicz J et al. 2012. Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes. PNAS 109:E2832–41
    [Google Scholar]
  25. Chih C-P, Lipton P, Roberts EL. 2001. Do active cerebral neurons really use lactate rather than glucose?. Trends Neurosci 24:573–78
    [Google Scholar]
  26. Clasadonte J, Scemes E, Wang Z, Boison D, Haydon PG. 2017. Connexin 43-mediated astroglial metabolic networks contribute to the regulation of the sleep-wake cycle. Neuron 95:1365–80.e5
    [Google Scholar]
  27. Collingridge GL, Peineau S, Howland JG, Wang YT. 2010. Long-term depression in the CNS. Nat. Rev. Neurosci. 11:459–73
    [Google Scholar]
  28. Corkrum M, Covelo A, Lines J, Bellocchio L, Pisansky M et al. 2020. Dopamine-evoked synaptic regulation in the nucleus accumbens requires astrocyte activity. Neuron 105:1036–47.e5
    [Google Scholar]
  29. Cui Y, Yang Y, Ni Z, Dong Y, Cai G et al. 2018. Astroglial Kir4.1 in the lateral habenula drives neuronal bursts in depression. Nature 554:323–27
    [Google Scholar]
  30. Das SC, Yamamoto BK, Hristov AM, Sari Y. 2015. Ceftriaxone attenuates ethanol drinking and restores extracellular glutamate concentration through normalization of GLT-1 in nucleus accumbens of male alcohol-preferring rats. Neuropharmacology 97:67–74
    [Google Scholar]
  31. De Pittà M, Brunel N, Volterra A. 2016. Astrocytes: orchestrating synaptic plasticity?. Neuroscience 323:43–61
    [Google Scholar]
  32. Deemyad T, Lüthi J, Spruston N. 2018. Astrocytes integrate and drive action potential firing in inhibitory subnetworks. Nat. Commun. 9:4336
    [Google Scholar]
  33. Dringen R, Gebhardt R, Hamprecht B. 1993. Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208–14
    [Google Scholar]
  34. Durkee CA, Covelo A, Lines J, Kofuji P, Aguilar J, Araque A. 2019. Gi/o protein-coupled receptors inhibit neurons but activate astrocytes and stimulate gliotransmission. Glia 67:1076–93
    [Google Scholar]
  35. Duvarci S, Pare D. 2014. Amygdala microcircuits controlling learned fear. Neuron 82:966–80
    [Google Scholar]
  36. Euston DR, Gruber AJ, McNaughton BL. 2012. The role of medial prefrontal cortex in memory and decision making. Neuron 76:1057–70
    [Google Scholar]
  37. Fiacco TA, McCarthy KD. 2018. Multiple lines of evidence indicate that gliotransmission does not occur under physiological conditions. J. Neurosci. 38:3–13
    [Google Scholar]
  38. Fischer KD, Houston ACW, Rebec GV. 2013. Role of the major glutamate transporter GLT1 in nucleus accumbens core versus shell in cue-induced cocaine-seeking behavior. J. Neurosci. 33:9319–27
    [Google Scholar]
  39. Fujita T, Chen MJ, Li B, Smith NA, Peng W et al. 2014. Neuronal transgene expression in dominant-negative SNARE mice. J. Neurosci. 34:16594–604
    [Google Scholar]
  40. Gao V, Suzuki A, Magistretti PJ, Lengacher S, Pollonini G et al. 2016. Astrocytic β2-adrenergic receptors mediate hippocampal long-term memory consolidation. PNAS 113:8526–31
    [Google Scholar]
  41. García-Cáceres C, Balland E, Prevot V, Luquet S, Woods SC et al. 2019. Role of astrocytes, microglia, and tanycytes in brain control of systemic metabolism. Nat. Neurosci. 22:7–14
    [Google Scholar]
  42. Gibbs ME, Hertz L. 2008. Inhibition of astrocytic energy metabolism by d-lactate exposure impairs memory. Neurochem. Int. 52:1012–18
    [Google Scholar]
  43. Gipson CD, Reissner KJ, Kupchik YM, Smith ACW, Stankeviciute N et al. 2013. Reinstatement of nicotine seeking is mediated by glutamatergic plasticity. PNAS 110:9124–29
    [Google Scholar]
  44. Gomez JA, Perkins JM, Beaudoin GM, Cook NB, Quraishi SA et al. 2019. Ventral tegmental area astrocytes orchestrate avoidance and approach behavior. Nat. Commun. 10:1455
    [Google Scholar]
  45. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF et al. 2010. Astrocytes control breathing through pH-dependent release of ATP. Science 329:571–75
    [Google Scholar]
  46. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY et al. 2009. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61:213–19
    [Google Scholar]
  47. Han H, Peng Y, Dong Z. 2015. d-Serine rescues the deficits of hippocampal long-term potentiation and learning and memory induced by sodium fluoroacetate. Pharmacol. Biochem. Behav. 133:51–56
    [Google Scholar]
  48. Han J, Kesner P, Metna-Laurent M, Duan T, Xu L et al. 2012. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148:1039–50
    [Google Scholar]
  49. Hansen KB, Yi F, Perszyk RE, Furukawa H, Wollmuth LP et al. 2018. Structure, function, and allosteric modulation of NMDA receptors. J. Gen. Physiol. 150:1081–105
    [Google Scholar]
  50. Hastings MH, Maywood ES, Brancaccio M. 2018. Generation of circadian rhythms in the suprachiasmatic nucleus. Nat. Rev. Neurosci. 19:453–69
    [Google Scholar]
  51. Henneberger C, Papouin T, Oliet SH, Rusakov DA. 2010. Long-term potentiation depends on release of d-serine from astrocytes. Nature 463:232–36
    [Google Scholar]
  52. Hyman SE, Malenka RC, Nestler EJ. 2006. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29:565–98
    [Google Scholar]
  53. Janak PH, Tye KM. 2015. From circuits to behaviour in the amygdala. Nature 517:284–92
    [Google Scholar]
  54. Jensen CJ, Demol F, Bauwens R, Kooijman R, Massie A et al. 2016. Astrocytic β2 adrenergic receptor gene deletion affects memory in aged mice. PLOS ONE 11:e0164721
    [Google Scholar]
  55. John CS, Smith KL, Van'T Veer A, Gompf HS, Carlezon WA et al. 2012. Blockade of astrocytic glutamate uptake in the prefrontal cortex induces anhedonia. Neuropsychopharmacology 37:2467–75
    [Google Scholar]
  56. Kakegawa W, Miyoshi Y, Hamase K, Matsuda S, Matsuda K et al. 2011. d-Serine regulates cerebellar LTD and motor coordination through the δ2 glutamate receptor. Nat. Neurosci. 14:603–11
    [Google Scholar]
  57. Kinoshita M, Hirayama Y, Fujishita K, Shibata K, Shinozaki Y et al. 2018. Anti-depressant fluoxetine reveals its therapeutic effect via astrocytes. EBioMedicine 32:72–83
    [Google Scholar]
  58. Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD et al. 2017. Engrams and circuits crucial for systems consolidation of a memory. Science 356:73–78
    [Google Scholar]
  59. Knackstedt LA, Melendez RI, Kalivas PW. 2010. Ceftriaxone restores glutamate homeostasis and prevents relapse to cocaine seeking. Biol. Psychiatry 67:81–84
    [Google Scholar]
  60. Kofuji P, Araque A. 2021. G-protein-coupled receptors in astrocyte–neuron communication. Neuroscience 456:7184
    [Google Scholar]
  61. Kol A, Adamsky A, Groysman M, Kreisel T, London M, Goshen I. 2020. Astrocytes contribute to remote memory formation by modulating hippocampal–cortical communication during learning. Nat. Neurosci. 23:1229–39
    [Google Scholar]
  62. Li K, Zhou T, Liao L, Yang Z, Wong C et al. 2013. βCaMKII in lateral habenula mediates core symptoms of depression. Science 341:1016–20
    [Google Scholar]
  63. Lines J, Martin ED, Kofuji P, Aguilar J, Araque A. 2020. Astrocytes modulate sensory-evoked neuronal network activity. Nat. Commun. 11:3689
    [Google Scholar]
  64. Magistretti PJ, Allaman I. 2018. Lactate in the brain: from metabolic end-product to signalling molecule. Nat. Rev. Neurosci. 19:235–49
    [Google Scholar]
  65. Martin R, Bajo-Graneras R, Moratalla R, Perea G, Araque A. 2015. Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways. Science 349:730–34
    [Google Scholar]
  66. Martin-Fernandez M, Jamison S, Robin LM, Zhao Z, Martin ED et al. 2017. Synapse-specific astrocyte gating of amygdala-related behavior. Nat. Neurosci. 20:1540–48
    [Google Scholar]
  67. Mason S. 2017. Lactate shuttles in neuroenergetics—homeostasis, allostasis and beyond. Front. Neurosci. 11:43
    [Google Scholar]
  68. Matsumoto M, Hikosaka O. 2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111–15
    [Google Scholar]
  69. Mederos S, Hernández-Vivanco A, Ramírez-Franco J, Martín-Fernández M, Navarrete M et al. 2019. Melanopsin for precise optogenetic activation of astrocyte-neuron networks. Glia 67:915–34
    [Google Scholar]
  70. Mederos S, Sanchez-Puelles C, Esparza J, Valero M, Ponomarenko A, Perea G. 2021. GABAergic signaling to astrocytes in prefrontal cortex sustains goal-directed behaviors. Nat. Neurosci. 24:8292
    [Google Scholar]
  71. Monai H, Ohkura M, Tanaka M, Oe Y, Konno A et al. 2016. Calcium imaging reveals glial involvement in transcranial direct current stimulation-induced plasticity in mouse brain. Nat. Commun. 7:11100
    [Google Scholar]
  72. Morquette P, Verdier D, Kadala A, Féthière J, Philippe AG et al. 2015. An astrocyte-dependent mechanism for neuronal rhythmogenesis. Nat. Neurosci. 18:844–54
    [Google Scholar]
  73. Mu Y, Bennett DV, Rubinov M, Narayan S, Yang C-T et al. 2019. Glia accumulate evidence that actions are futile and suppress unsuccessful behavior. Cell 178:27–43.e19
    [Google Scholar]
  74. Nagai J, Rajbhandari AK, Gangwani MR, Hachisuka A, Coppola G et al. 2019. Hyperactivity with disrupted attention by activation of an astrocyte synaptogenic cue. Cell 177:1280–92.e20
    [Google Scholar]
  75. Navarrete M, Cuartero MI, Palenzuela R, Draffin JE, Konomi A et al. 2019. Astrocytic p38α MAPK drives NMDA receptor-dependent long-term depression and modulates long-term memory. Nat. Commun. 10:2968
    [Google Scholar]
  76. Navarrete M, Perea G, de Sevilla DF, Gómez-Gonzalo M, Núñez A et al. 2012. Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLOS Biol 10:e1001259
    [Google Scholar]
  77. Nestler EJ, Lüscher C. 2019. The molecular basis of drug addiction: linking epigenetic to synaptic and circuit mechanisms. Neuron 102:48–59
    [Google Scholar]
  78. Nicoll RA. 2017. A brief history of long-term potentiation. Neuron 93:281–90
    [Google Scholar]
  79. O'Donnell J, Zeppenfeld D, McConnell E, Pena S, Nedergaard M. 2012. Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem. Res. 37:2496–512
    [Google Scholar]
  80. Oe Y, Wang X, Patriarchi T, Konno A, Ozawa K et al. 2020. Distinct temporal integration of noradrenaline signaling by astrocytic second messengers during vigilance. Nat. Commun. 11:471
    [Google Scholar]
  81. Okada Y, Sasaki T, Oku Y, Takahashi N, Seki M et al. 2012. Preinspiratory calcium rise in putative pre-Bötzinger complex astrocytes. J. Physiol. 590:4933–44
    [Google Scholar]
  82. Oliveira JF, Sardinha VM, Guerra-Gomes S, Araque A, Sousa N 2015. Do stars govern our actions? Astrocyte involvement in rodent behavior. Trends Neurosci 38:535–49
    [Google Scholar]
  83. Orellana JA, Stehberg J. 2014. Hemichannels: new roles in astroglial function. Front. Physiol. 5:193
    [Google Scholar]
  84. Padmashri R, Suresh A, Boska MD, Dunaevsky A. 2015. Motor-skill learning is dependent on astrocytic activity. Neural Plast 2015.938023
    [Google Scholar]
  85. Panatier A, Vallee J, Haber M, Murai KK, Lacaille JC, Robitaille R. 2011. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785–98
    [Google Scholar]
  86. Papouin T, Henneberger C, Rusakov DA, Oliet SHR. 2017. Astroglial versus neuronal d-serine: fact checking. Trends Neurosci 40:517–20
    [Google Scholar]
  87. Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE. 2014. Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82:1263–70
    [Google Scholar]
  88. Pelluru D, Konadhode RR, Bhat NR, Shiromani PJ. 2016. Optogenetic stimulation of astrocytes in the posterior hypothalamus increases sleep at night in C57BL/6J mice. Eur. J. Neurosci. 43:1298–306
    [Google Scholar]
  89. Perea G, Araque A. 2005. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J. Neurosci. 25:2192–203
    [Google Scholar]
  90. 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
    [Google Scholar]
  91. Perez-Alvarez A, Navarrete M, Covelo A, Martin ED, Araque A. 2014. Structural and functional plasticity of astrocyte processes and dendritic spine interactions. J. Neurosci. 34:12738–44
    [Google Scholar]
  92. Petravicz J, Boyt KM, McCarthy KD. 2014. Astrocyte IP3R2-dependent Ca2+ signaling is not a major modulator of neuronal pathways governing behavior. Front. Behav. Neurosci. 8:384
    [Google Scholar]
  93. Pinto-Duarte A, Roberts AJ, Ouyang K, Sejnowski TJ. 2019. Impairments in remote memory caused by the lack of Type 2 IP3 receptors. Glia 67:1976–89
    [Google Scholar]
  94. Prolo LM, Takahashi JS, Herzog ED. 2005. Circadian rhythm generation and entrainment in astrocytes. J. Neurosci. 25:404–8
    [Google Scholar]
  95. Rash JE, Yasumura T, Dudek FE, Nagy JI. 2001. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 21:1983–2000
    [Google Scholar]
  96. Reissner KJ, Brown RM, Spencer S, Tran PK, Thomas CA, Kalivas PW. 2014. Chronic administration of the methylxanthine propentofylline impairs reinstatement to cocaine by a GLT-1-dependent mechanism. Neuropsychopharmacology 39:499–506
    [Google Scholar]
  97. Reissner KJ, Gipson CD, Tran PK, Knackstedt LA, Scofield MD, Kalivas PW. 2015. Glutamate transporter GLT-1 mediates N-acetylcysteine inhibition of cocaine reinstatement. Addict. Biol. 20:316–23
    [Google Scholar]
  98. Ressler KJ. 2010. Amygdala activity, fear, and anxiety: modulation by stress. Biol. Psychiatry 67:1117–19
    [Google Scholar]
  99. Robin LM, Oliveira da Cruz JF, Langlais VC, Martin-Fernandez M, Metna-Laurent M et al. 2018. Astroglial CB1 receptors determine synaptic d-serine availability to enable recognition memory. Neuron 98:935–44.e5
    [Google Scholar]
  100. Rodrigues SM, Schafe GE, LeDoux JE. 2004. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75–91
    [Google Scholar]
  101. Saab AS, Neumeyer A, Jahn HM, Cupido A, Šimek AAM et al. 2012. Bergmann glial AMPA receptors are required for fine motor coordination. Science 337:749–53
    [Google Scholar]
  102. Savtchouk I, Volterra A. 2018. Gliotransmission: beyond black-and-white. J. Neurosci. 38:14–25
    [Google Scholar]
  103. Schummers J, Yu H, Sur M. 2008. Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638–43
    [Google Scholar]
  104. Scofield MD, Kalivas PW. 2014. Astrocytic dysfunction and addiction: consequences of impaired glutamate homeostasis. Neuroscientist 20:610–22
    [Google Scholar]
  105. Sheikhbahaei S, Turovsky EA, Hosford PS, Hadjihambi A, Theparambil SM et al. 2018. Astrocytes modulate brainstem respiratory rhythm-generating circuits and determine exercise capacity. Nat. Commun. 9:370
    [Google Scholar]
  106. Shen H-W, Scofield MD, Boger H, Hensley M, Kalivas PW. 2014. Synaptic glutamate spillover due to impaired glutamate uptake mediates heroin relapse. J. Neurosci. 34:5649–57
    [Google Scholar]
  107. Shigetomi E, Bushong EA, Haustein MD, Tong X, Jackson-Weaver O et al. 2013. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J. Gen. Physiol. 141:633–47
    [Google Scholar]
  108. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. 1991. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726–29
    [Google Scholar]
  109. Srinivasan R, Huang BS, Venugopal S, Johnston AD, Chai H et al. 2015. Ca2+ signaling in astrocytes from Ip3r2−/− mice in brain slices and during startle responses in vivo. Nat. Neurosci 18:708–17
    [Google Scholar]
  110. Stehberg J, Moraga-Amaro R, Salazar C, Becerra A, Echeverría C et al. 2012. Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J 26:3649–57
    [Google Scholar]
  111. Steinman MQ, Gao V, Alberini CM. 2016. The role of lactate-mediated metabolic coupling between astrocytes and neurons in long-term memory formation. Front. Integr. Neurosci. 10:10
    [Google Scholar]
  112. Stobart JL, Ferrari KD, Barrett MJP, Glück C, Stobart MJ et al. 2018. Cortical circuit activity evokes rapid astrocyte calcium signals on a similar timescale to neurons. Neuron 98:726–35.e4
    [Google Scholar]
  113. Sun J-D, Liu Y, Yuan Y-H, Li J, Chen N-H. 2012. Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats. Neuropsychopharmacology 37:1305–20
    [Google Scholar]
  114. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH et al. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–23
    [Google Scholar]
  115. Tang F, Lane S, Korsak A, Paton JFR, Gourine AV et al. 2014. Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat. Commun. 5:3284
    [Google Scholar]
  116. Takata N, Mishima T, Hisatsune C, Nagai T, Ebisui E et al. 2011. Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J. Neurosci. 31:18155–65
    [Google Scholar]
  117. Tso CF, Simon T, Greenlaw AC, Puri T, Mieda M, Herzog ED. 2017. Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr. Biol. 27:1055–61
    [Google Scholar]
  118. Wang J, Tu J, Cao B, Mu L, Yang X et al. 2017. Astrocytic l-lactate signaling facilitates amygdala-anterior cingulate cortex synchrony and decision making in rats. Cell Rep 21:2407–18
    [Google Scholar]
  119. Welsh DK, Takahashi JS, Kay SA. 2010. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72:551–77
    [Google Scholar]
  120. Williams KW, Elmquist JK. 2012. From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior. Nat. Neurosci. 15:1350–55
    [Google Scholar]
  121. Wolosker H, Balu DT, Coyle JT. 2016. The rise and fall of the d-serine-mediated gliotransmission hypothesis. Trends Neurosci 39:712–21
    [Google Scholar]
  122. Woo J, Min JO, Kang D-S, Kim YS, Jung GH et al. 2018. Control of motor coordination by astrocytic tonic GABA release through modulation of excitation/inhibition balance in cerebellum. PNAS 115:5004–9
    [Google Scholar]
  123. Yang L, Qi Y, Yang Y. 2015. Astrocytes control food intake by inhibiting AGRP neuron activity via adenosine A1 receptors. Cell Rep 11:798–807
    [Google Scholar]
  124. Yang Y, Ge W, Chen Y, Zhang Z, Shen W et al. 2003. Contribution of astrocytes to hippocampal long-term potentiation through release of d-serine. PNAS 100:15194–99
    [Google Scholar]
  125. Zhang Y, Xue Y, Meng S, Luo Y, Liang J et al. 2016. Inhibition of lactate transport erases drug memory and prevents drug relapse. Biol. Psychiatry 79:928–39
    [Google Scholar]
  126. Zhang Z, Gong N, Wang W, Xu L, Xu T-L. 2008. Bell-shaped d-serine actions on hippocampal long-term depression and spatial memory retrieval. Cereb. Cortex 18:2391–401
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-101920-112225
Loading
/content/journals/10.1146/annurev-neuro-101920-112225
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error