Astrocytes Render Memory Flexible by Releasing D-Serine and Regulating NMDA Receptor Tone in the Hippocampus

References

1. • Tello-Ramos M.C.
   • Branch C.L.
   • Kozlovsky D.Y.
   • Pitera A.M.
   • Pravosudov V.V.
   Spatial memory and cognitive flexibility trade-offs: To be or not to be flexible, that is the question.
   Anim Behav. 2019; 147: 129-136
   View in Article

   • Google Scholar
2. • D’Cruz A.M.
   • Ragozzino M.E.
   • Mosconi M.W.
   • Shrestha S.
   • Cook E.H.
   • Sweeney J.A.
   Reduced behavioral flexibility in autism spectrum disorders.
   Neuropsychology. 2013; 27: 152-160
   View in Article

   • Google Scholar
3. • Wobrock T.
   • Ecker U.K.H.
   • Scherk H.
   • Schneider-Axmann T.
   • Falkai P.
   • Gruber O.
   Cognitive impairment of executive function as a core symptom of schizophrenia.
   World J Biol Psychiatry. 2009; 10: 442-451
   View in Article

   • Google Scholar
4. • Etienne V.
   • Marin-Lamellet C.
   • Laurent B.
   Mental flexibility impairment in drivers with early Alzheimer’s disease: A simulator-based study.
   IATSS Res. 2013; 37: 16-20
   View in Article

   • Google Scholar
5. • Guarino A.
   • Favieri F.
   • Boncompagni I.
   • Agostini F.
   • Cantone M.
   • Casagrande M.
   Executive functions in Alzheimer disease: A systematic review.
   Front Aging Neurosci. 2019; 10: 437
   View in Article

   • Google Scholar
6. • Lee G.
   • Zhou Y.
   NMDAR hypofunction animal models of schizophrenia.
   Front Mol Neurosci. 2019; 12: 185
   View in Article

   • Google Scholar
7. • Gandal M.J.
   • Anderson R.L.
   • Billingslea E.N.
   • Carlson G.C.
   • Roberts T.P.L.
   • Siegel S.J.
   Mice with reduced NMDA receptor expression: More consistent with autism than schizophrenia?.
   Genes Brain Behav. 2012; 11: 740-750
   View in Article

   • Google Scholar
8. • Huang Y.J.
   • Lin C.H.
   • Lane H.Y.
   • Tsai G.E.
   NMDA neurotransmission dysfunction in behavioral and psychological symptoms of Alzheimer’s disease.
   Curr Neuropharmacol. 2012; 10: 272-285
   View in Article

   • Google Scholar
9. • Nicholls R.E.
   • Alarcon J.M.
   • Malleret G.
   • Carroll R.C.
   • Grody M.
   • Vronskaya S.
   • Kandel E.R.
   Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility.
   Neuron. 2008; 58: 104-117
   View in Article

   • Google Scholar
10. • Li J.
    • Chai A.
    • Wang L.
    • Ma Y.
    • Wu Z.
    • Yu H.
    • et al.
    Synaptic P-Rex1 signaling regulates hippocampal long-term depression and autism-like social behavior.
    Proc Natl Acad Sci U S A. 2015; 112: E6964-E6972
    View in Article

    • Google Scholar
11. • Morice E.
    • Billard J.M.
    • Denis C.
    • Mathieu F.
    • Betancur C.
    • Epelbaum J.
    • et al.
    Parallel loss of hippocampal LTD and cognitive flexibility in a genetic model of hyperdopaminergia.
    Neuropsychopharmacology. 2007; 32: 2108-2116
    View in Article

    • Google Scholar
12. • Duffy S.
    • Labrie V.
    • Roder J.C.
    D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning.
    Neuropsychopharmacology. 2008; 33: 1004-1018
    View in Article

    • Google Scholar
13. • Izquierdo A.
    • Brigman J.L.
    • Radke A.K.
    • Rudebeck P.H.
    • Holmes A.
    The neural basis of reversal learning: An updated perspective.
    Neuroscience. 2017; 345: 12-26
    View in Article

    • Google Scholar
14. • Dudek S.M.
    • Bear M.F.
    Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade.
    Proc Natl Acad Sci U S A. 1992; 89: 4363-4367
    View in Article

    • Google Scholar
15. • Rutten K.
    • Wallace T.L.
    • Works M.
    • Prickaerts J.
    • Blokland A.
    • Novak T.J.
    • et al.
    Enhanced long-term depression and impaired reversal learning in phosphodiesterase 4B-knockout (PDE4B−/−) mice.
    Neuropharmacology. 2011; 61: 138-147
    View in Article

    • Google Scholar
16. • Zhang M.
    • Wang H.
    Mice overexpressing type 1 adenylyl cyclase show enhanced spatial memory flexibility in the absence of intact synaptic long-term depression.
    Learn Mem. 2013; 20: 352-357
    View in Article

    • Google Scholar
17. • Zhang Z.
    • Gong N.
    • Wang W.
    • Xu L.
    • Xu T.L.
    Bell-shaped D-serine actions on hippocampal long-term depression and spatial memory retrieval.
    Cereb Cortex. 2008; 18: 2391-2401
    View in Article

    • Google Scholar
18. • Labrie V.
    • Duffy S.
    • Wang W.
    • Barger S.W.
    • Baker G.B.
    • Roder J.C.
    Genetic inactivation of D-amino acid oxidase enhances extinction and reversal learning in mice.
    Learn Mem. 2008; 16: 28-37
    View in Article

    • Google Scholar
19. • Papouin T.
    • Henneberger C.
    • Rusakov D.A.
    • Oliet S.H.R.
    Astroglial versus neuronal D-serine: Fact checking.
    Trends Neurosci. 2017; 40: 517-520
    View in Article

    • Google Scholar
20. • Wolosker H.
    • Balu D.T.
    • Coyle J.T.
    Astroglial versus neuronal D-serine: Check your controls.
    Trends Neurosci. 2017; 40: 520-522
    View in Article

    • Google Scholar
21. • Shen W.
    • Nikolic L.
    • Meunier C.
    • Pfrieger F.
    • Audinat E.
    An autocrine purinergic signaling controls astrocyte-induced neuronal excitation.
    Sci Rep. 2017; 7: 11280
    View in Article

    • Google Scholar
22. • Navarrete M.
    • Cuartero M.I.
    • Palenzuela R.
    • Draffin J.E.
    • Konomi A.
    • Serra I.
    • et al.
    Astrocytic p38α MAPK drives NMDA receptor-dependent long-term depression and modulates long-term memory.
    Nat Commun. 2019; 10: 2968
    View in Article

    • Google Scholar
23. • Oh S.J.
    • Lee C.J.
    Distribution and function of the bestrophin-1 (Best1) channel in the brain.
    Exp Neurobiol. 2017; 26: 113-121
    View in Article

    • Google Scholar
24. • Woo D.H.
    • Han K.S.
    • Shim J.W.
    • Yoon B.E.
    • Kim E.
    • Bae J.Y.
    • et al.
    TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation.
    Cell. 2012; 151: 25-40
    View in Article

    • Google Scholar
25. • Park H.
    • Han K.S.
    • Oh S.J.
    • Jo S.
    • Woo J.
    • Yoon B.E.
    • Lee C.J.
    High glutamate permeability and distal localization of Best1 channel in CA1 hippocampal astrocyte.
    Mol Brain. 2013; 6: 54
    View in Article

    • Google Scholar
26. • Duffy S.
    • MacVicar B.A.
    Adrenergic calcium signaling in astrocyte networks within the hippocampal slice.
    J Neurosci. 1995; 15: 5535-5550
    View in Article

    • Google Scholar
27. • Scheiderer C.L.
    • Dobrunz L.E.
    • McMahon L.L.
    Novel form of long-term synaptic depression in rat hippocampus induced by activation of alpha 1 adrenergic receptors.
    J Neurophysiol. 2004; 91: 1071-1077
    View in Article

    • Google Scholar
28. • Lee H.K.
    • Kameyama K.
    • Huganir R.L.
    • Bear M.F.
    NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus.
    Neuron. 1998; 21: 1151-1162
    View in Article

    • Google Scholar
29. • Rorabaugh J.M.
    • Chalermpalanupap T.
    • Botz-Zapp C.A.
    • Fu V.M.
    • Lembeck N.A.
    • Cohen R.M.
    • Weinshenker D.
    Chemogenetic locus coeruleus activation restores reversal learning in a rat model of Alzheimer’s disease.
    Brain. 2017; 140: 3023-3038
    View in Article

    • Google Scholar
30. • Pinto-Duarte A.
    • Roberts A.J.
    • Ouyang K.
    • Sejnowski T.J.
    Impairments in remote memory caused by the lack of type 2 IP3 receptors.
    Glia. 2019; 67: 1976-1989
    View in Article

    • Google Scholar
31. • Chen J.
    • Tan Z.
    • Zeng L.
    • Zhang X.
    • He Y.
    • Gao W.
    • et al.
    Heterosynaptic long-term depression mediated by ATP released from astrocytes.
    Glia. 2013; 61: 178-191
    View in Article

    • Google Scholar
32. • Chen J.Y.
    • Lonjers P.
    • Lee C.
    • Chistiakova M.
    • Volgushev M.
    • Bazhenov M.
    Heterosynaptic plasticity prevents runaway synaptic dynamics.
    J Neurosci. 2013; 33: 15915-15929
    View in Article

    • Google Scholar
33. • Abraham W.C.
    • Bear M.F.
    Metaplasticity: The plasticity of synaptic plasticity.
    Trends Neurosci. 1996; 19: 126-130
    View in Article

    • Google Scholar
34. • Hulme S.R.
    • Jones O.D.
    • Raymond C.R.
    • Sah P.
    • Abraham W.C.
    Mechanisms of heterosynaptic metaplasticity.
    Philos Trans R Soc Lond B Biol Sci. 2013; 369: 20130148
    View in Article

    • Google Scholar
35. • Kwak H.
    • Koh W.
    • Kim S.
    • Song K.
    • Shin J.I.
    • Lee J.M.
    • et al.
    Astrocytes control sensory acuity via tonic inhibition in the thalamus.
    Neuron. 2020; 108: 691-706.e10
    View in Article

    • Google Scholar
36. • Lee C.J.
    • Mannaioni G.
    • Yuan H.
    • Woo D.H.
    • Gingrich M.B.
    • Traynelis S.F.
    Astrocytic control of synaptic NMDA receptors.
    J Physiol. 2007; 581: 1057-1081
    View in Article

    • Google Scholar
37. • Park M.
    • Kim C.H.
    • Jo S.
    • Kim E.J.
    • Rhim H.
    • Lee C.J.
    • et al.
    Chronic stress alters spatial representation and bursting patterns of place cells in behaving mice.
    Sci Rep. 2015; 5: 16235
    View in Article

    • Google Scholar
38. • Sahlender D.A.
    • Savtchouk I.
    • Volterra A.
    What do we know about gliotransmitter release from astrocytes?.
    Philos Trans R Soc Lond B Biol Sci. 2014; 369: 20130592
    View in Article

    • Google Scholar
39. • Semyanov A.
    • Henneberger C.
    • Agarwal A.
    Making sense of astrocytic calcium signals—From acquisition to interpretation.
    Nat Rev Neurosci. 2020; 21: 551-564
    View in Article

    • Google Scholar
40. • Lalo U.
    • Koh W.
    • Lee C.J.
    • Pankratov Y.
    The tripartite glutamatergic synapse.
    Neuropharmacology. 2021; 199: 108758
    View in Article

    • Google Scholar
41. • Le Meur K.
    • Galante M.
    • Angulo M.C.
    • Audinat E.
    Tonic activation of NMDA receptors by ambient glutamate of non-synaptic origin in the rat hippocampus.
    J Physiol. 2007; 580: 373-383
    View in Article

    • Google Scholar
42. • Marmorstein L.Y.
    • Wu J.
    • McLaughlin P.
    • Yocom J.
    • Karl M.O.
    • Neussert R.
    • et al.
    The light peak of the electroretinogram is dependent on voltage-gated calcium channels and antagonized by bestrophin (best-1).
    J Gen Physiol. 2006; 127: 577-589
    View in Article

    • Google Scholar
43. • Park H.
    • Han K.S.
    • Seo J.
    • Lee J.
    • Dravid S.M.
    • Woo J.
    • et al.
    Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors [published correction appears in Mol Brain 2021; 14:103].
    Mol Brain. 2015; 8: 7
    View in Article

    • Google Scholar
44. • Papouin T.
    • Ladépêche L.
    • Ruel J.
    • Sacchi S.
    • Labasque M.
    • Hanini M.
    • et al.
    Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists.
    Cell. 2012; 150: 633-646
    View in Article

    • Google Scholar
45. • Malva J.O.
    • Carvalho A.P.
    • Carvalho C.M.
    Modulation of dopamine and noradrenaline release and of intracellular Ca2+ concentration by presynaptic glutamate receptors in hippocampus.
    Br J Pharmacol. 1994; 113: 1439-1447
    View in Article

    • Google Scholar
46. • Howells F.M.
    • Russell V.A.
    Glutamate-stimulated release of norepinephrine in hippocampal slices of animal models of attention-deficit/hyperactivity disorder (spontaneously hypertensive rat) and depression/anxiety-like behaviours (Wistar-Kyoto rat).
    Brain Res. 2008; 1200: 107-115
    View in Article

    • Google Scholar
47. • Feng J.
    • Zhang C.
    • Lischinsky J.E.
    • Jing M.
    • Zhou J.
    • Wang H.
    • et al.
    A genetically encoded fluorescent sensor for rapid and specific in vivo detection of norepinephrine.
    Neuron. 2019; 102: 745-761.e8
    View in Article

    • Google Scholar
48. • Scanziani M.
    • Nicoll R.A.
    • Malenka R.C.
    Heterosynaptic long-term depression in the hippocampus.
    J Physiol Paris. 1996; 90: 165-166
    View in Article

    • Google Scholar
49. • Dudek S.M.
    • Bear M.F.
    Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus.
    J Neurosci. 1993; 13: 2910-2918
    View in Article

    • Google Scholar
50. • Petravicz J.
    • Fiacco T.A.
    • McCarthy K.D.
    Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity.
    J Neurosci. 2008; 28: 4967-4973
    View in Article

    • Google Scholar
51. • Okubo Y.
    • Kanemaru K.
    • Suzuki J.
    • Kobayashi K.
    • Hirose K.
    • Iino M.
    Inositol 1,4,5-trisphosphate receptor type 2-independent Ca ²⁺ release from the endoplasmic reticulum in astrocytes.
    Glia. 2019; 67: 113-124
    View in Article

    • Google Scholar
52. • Shigetomi E.
    • Jackson-Weaver O.
    • Huckstepp R.T.
    • O’Dell T.J.
    • Khakh B.S.
    TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release.
    J Neurosci. 2013; 33: 10143-10153
    View in Article

    • Google Scholar
53. • Rungta R.L.
    • Bernier L.P.
    • Dissing-Olesen L.
    • Groten C.J.
    • LeDue J.M.
    • Ko R.
    • et al.
    Ca ²⁺ transients in astrocyte fine processes occur via Ca ²⁺ influx in the adult mouse hippocampus.
    Glia. 2016; 64: 2093-2103
    View in Article

    • Google Scholar
54. • Oh S.J.
    • Lee J.M.
    • Kim H.B.
    • Lee J.
    • Han S.
    • Bae J.Y.
    • et al.
    Ultrasonic neuromodulation via astrocytic TRPA1 [published correction appears in Curr Biol 2020; 30:948.
    Curr Biol. 2019; 29: 3386-3401.e8
    View in Article

    • Google Scholar
55. • Benneyworth M.A.
    • Li Y.
    • Basu A.C.
    • Bolshakov V.Y.
    • Coyle J.T.
    Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons.
    Cell Mol Neurobiol. 2012; 32: 613-624
    View in Article

    • Google Scholar
56. • Sason H.
    • Billard J.M.
    • Smith G.P.
    • Safory H.
    • Neame S.
    • Kaplan E.
    • et al.
    Asc-1 transporter regulation of synaptic activity via the tonic release of d-serine in the forebrain.
    Cereb Cortex. 2017; 27: 1573-1587
    View in Article

    • Google Scholar
57. • Papouin T.
    • Dunphy J.M.
    • Tolman M.
    • Dineley K.T.
    • Haydon P.G.
    Septal cholinergic neuromodulation tunes the astrocyte-dependent gating of hippocampal NMDA receptors to wakefulness.
    Neuron. 2017; 94: 840-854.e7
    View in Article

    • Google Scholar
58. • Henneberger C.
    • Papouin T.
    • Oliet S.H.R.
    • Rusakov D.A.
    Long-term potentiation depends on release of D-serine from astrocytes.
    Nature. 2010; 463: 232-236
    View in Article

    • Google Scholar
59. • Rosenberg D.
    • Artoul S.
    • Segal A.C.
    • Kolodney G.
    • Radzishevsky I.
    • Dikopoltsev E.
    • et al.
    Neuronal D-serine and glycine release via the Asc-1 transporter regulates NMDA receptor-dependent synaptic activity.
    J Neurosci. 2013; 33: 3533-3544
    View in Article

    • Google Scholar
60. • Citri A.
    • Malenka R.C.
    Synaptic plasticity: Multiple forms, functions, and mechanisms.
    Neuropsychopharmacology. 2008; 33: 18-41
    View in Article

    • Google Scholar
61. • Nabavi S.
    • Kessels H.W.
    • Alfonso S.
    • Aow J.
    • Fox R.
    • Malinow R.
    Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression.
    Proc Natl Acad Sci U S A. 2013; 110: 4027-4032
    View in Article

    • Google Scholar
62. • Ottestad-Hansen S.
    • Hu Q.X.
    • Follin-Arbelet V.V.
    • Bentea E.
    • Sato H.
    • Massie A.
    • et al.
    The cystine-glutamate exchanger (xCT, Slc7a11) is expressed in significant concentrations in a subpopulation of astrocytes in the mouse brain.
    Glia. 2018; 66: 951-970
    View in Article

    • Google Scholar
63. • Araque A.
    • Li N.
    • Doyle R.T.
    • Haydon P.G.
    SNARE protein-dependent glutamate release from astrocytes.
    J Neurosci. 2000; 20: 666-673
    View in Article

    • Google Scholar
64. • Han Y.E.
    • Kwon J.
    • Won J.
    • An H.
    • Jang M.W.
    • Woo J.
    • et al.
    Tweety-homolog (Ttyh) family encodes the pore-forming subunits of the swelling-dependent volume-regulated anion channel (VRACswell) in the brain.
    Exp Neurobiol. 2019; 28: 183-215
    View in Article

    • Google Scholar
65. • Yang J.
    • Vitery M.D.C.
    • Chen J.
    • Osei-Owusu J.
    • Chu J.
    • Qiu Z.
    Glutamate-releasing SWELL1 channel in astrocytes modulates synaptic transmission and promotes brain damage in stroke.
    Neuron. 2019; 102: 813-827.e6
    View in Article

    • Google Scholar
66. • Lalo U.
    • Rasooli-Nejad S.
    • Bogdanov A.
    • More L.
    • Koh W.
    • Muller J.
    • et al.
    Synergy between vesicular and non-vesicular gliotransmission regulates synaptic plasticity and working memory.
    bioRxiv. 2021; https://doi.org/10.1101/2021.03.25.437028
    View in Article

    • Google Scholar
67. • Povysheva N.V.
    • Johnson J.W.
    Tonic NMDA receptor-mediated current in prefrontal cortical pyramidal cells and fast-spiking interneurons.
    J Neurophysiol. 2012; 107: 2232-2243
    View in Article

    • Google Scholar
68. • Ghersi C.
    • Bonfanti A.
    • Manzari B.
    • Feligioni M.
    • Raiteri M.
    • Pittaluga A.
    Pharmacological heterogeneity of release-regulating presynaptic AMPA/kainate receptors in the rat brain: Study with receptor antagonists.
    Neurochem Int. 2003; 42: 283-292
    View in Article

    • Google Scholar
69. • Atzori M.
    • Cuevas-Olguin R.
    • Esquivel-Rendon E.
    • Garcia-Oscos F.
    • Salgado-Delgado R.C.
    • Saderi N.
    • et al.
    Locus ceruleus norepinephrine release: A central regulator of CNS spatio-temporal activation?.
    Front Synaptic Neurosci. 2016; 8: 25
    View in Article

    • Google Scholar
70. • Jacobowitz D.M.
    Hypothesis for the local control of norepinephrine release.
    in: Usdin E. Kopin I.J. Barchas J. Catecholamines: Basic and Clinical Frontiers, Proceedings of the Fourth International Catecholamine Symposium, Pacific Grove, California, September 17-22, 1978. Pergamon, New York1979: 1792-1794
    View in Article

    • Google Scholar
71. • Serrano A.
    • Haddjeri N.
    • Lacaille J.C.
    • Robitaille R.
    GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression.
    J Neurosci. 2006; 26: 5370-5382
    View in Article

    • Google Scholar
72. • Bushong E.A.
    • Martone M.E.
    • Jones Y.Z.
    • Ellisman M.H.
    Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains.
    J Neurosci. 2002; 22: 183-192
    View in Article

    • Google Scholar
73. • Kim J.I.
    • Lee H.R.
    • Sim S.E.
    • Baek J.
    • Yu N.K.
    • Choi J.H.
    • et al.
    PI3Kγ is required for NMDA receptor-dependent long-term depression and behavioral flexibility.
    Nat Neurosci. 2011; 14: 1447-1454
    View in Article

    • Google Scholar
74. • Dong Z.
    • Bai Y.
    • Wu X.
    • Li H.
    • Gong B.
    • Howland J.G.
    • et al.
    Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze.
    Neuropharmacology. 2013; 64: 65-73
    View in Article

    • Google Scholar
75. • Do-Monte F.H.M.
    • Allensworth M.
    • Carobrez A.P.
    Impairment of contextual conditioned fear extinction after microinjection of alpha-1-adrenergic blocker prazosin into the medial prefrontal cortex.
    Behav Brain Res. 2010; 211: 89-95
    View in Article

    • Google Scholar
76. • Homan P.
    • Lin Q.
    • Murrough J.W.
    • Soleimani L.
    • Bach D.R.
    • Clem R.L.
    • Schiller D.
    Prazosin during threat discrimination boosts memory of the safe stimulus.
    Learn Mem. 2017; 24: 597-601
    View in Article

    • Google Scholar
77. • Boone K.B.
    • Ghaffarian S.
    • Lesser I.M.
    • Hill-Gutierrez E.
    • Berman N.G.
    Wisconsin Card Sorting Test performance in healthy, older adults: Relationship to age, sex, education, and IQ.
    J Clin Psychol. 1993; 49: 54-60
    View in Article

    • Google Scholar
78. • Dezfuli G.
    • Martin L.
    • Olson T.
    • Kellar K.J.
    The decline of glutamate-stimulated norepinephrine release in aging rat brain.
    FASEB J. 2019; 33 (501.511–501.511)
    View in Article

    • Google Scholar
79. • Matchett B.J.
    • Grinberg L.T.
    • Theofilas P.
    • Murray M.E.
    The mechanistic link between selective vulnerability of the locus coeruleus and neurodegeneration in Alzheimer’s disease.
    Acta Neuropathol. 2021; 141: 631-650
    View in Article

    • Google Scholar