Motor-skill learning is dependent on astrocytic activity

Neural Plasticity

Volumn 2015, Issue , 2015, Pages

  Padmashri, Ragunathan ^a   Suresh, Anand ^a   Boska, Michael D ^b   Dunaevsky, Anna ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; DEXTRO SERINE; FLUOROCITRIC ACID; ANTIESTROGEN; ANTIMETABOLITE; CITRIC ACID; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; IP3R2 PROTEIN, MOUSE; SERINE; TAMOXIFEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CELL ACTIVITY; CONTROLLED STUDY; FORELIMB; IN VIVO STUDY; LEARNING; LEARNING DISORDER; MALE; MOTOR PERFORMANCE; MOTOR SKILL LEARNING; MOUSE; NONHUMAN; SYNAPTOSOME; TASK PERFORMANCE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; IN VITRO STUDY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; LONG TERM POTENTIATION; MUTATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SYNAPTIC TRANSMISSION;

ANIMALS; ANTIMETABOLITES; ASTROCYTES; CITRATES; ESTROGEN ANTAGONISTS; FORELIMB; IN VITRO TECHNIQUES; INJECTIONS, INTRAVENTRICULAR; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LEARNING; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MOTOR SKILLS; MUTATION; PSYCHOMOTOR PERFORMANCE; RECEPTORS, AMPA; SERINE; SYNAPTIC TRANSMISSION; TAMOXIFEN;

EID: 84939627512     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2015/938023     Document Type: Article

References (67)

1. C. Eroglu, "The role of astrocyte-secreted matricellular proteins in central nervous systemdevelopment and function, " Journal of Cell Communication and Signaling, vol. 3, no. 3-4, pp. 167-176, 2009.
2. S. B. Achour and O. Pascual, "Astrocyte-neuron communication: functional consequences, " Neurochemical Research, vol. 37, no. 11, pp. 2464-2473, 2012.
3. M. M. Halassa and P. G. Haydon, "Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior, " Annual Review of Physiology, vol. 72, pp. 335-355, 2010.
4. C. Agulhon, J. Petravicz, A. B. McMullen et al., "What is the role of astrocyte calcium in neurophysiology?" Neuron, vol. 59, no. 6, pp. 932-946, 2008.
5. J. Petravicz, T. A. Fiacco, and K. D. McCarthy, "Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity, " The Journal of Neuroscience, vol. 28, no. 19, pp. 4967-4973, 2008.
6. V. Parpura, T. A. Basarsky, F. Liu, K. Jeftinija, S. Jeftinija, and P. G. Haydon, "Glutamate-mediated astrocyte-neuron signalling, " Nature, vol. 369, no. 6483, pp. 744-747, 1994.
7. L. Pasti, A. Volterra, T. Pozzan, and G. Carmignoto, "Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ, " The Journal of Neuroscience, vol. 17, no. 20, pp. 7817-7830, 1997.
8. O. Pascual, K. B. Casper, C. Kubera et al., "Astrocytic purinergic signaling coordinates synaptic networks, " Science, vol. 310, no. 5745, pp. 113-116, 2005.
9. Q.-S. Liu, Q. Xu, G. Arcuino, J. Kang, and M. Nedergaard, "Astrocyte-mediated activation of neuronal kainate receptors, " Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3172-3177, 2004.
10. E. Shigetomi, O. Jackson-Weaver, R. T. Huckstepp, T. J. O'Dell, and B. S. Khakh, "TRPA1 channels are regulators of astrocyte basal calciumlevels and long-termpotentiation via constitutive d-serine release, " The Journal of Neuroscience, vol. 33, no. 24, pp. 10143-10153, 2013.
11. J.-P. Mothet, A. T. Parent, H. Wolosker et al., "D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor, " Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4926-4931, 2000.
12. A. Panatier, D. T. Theodosis, J.-P. Mothet et al., "Glia-derivedDserine controls NMDA receptor activity and synaptic memory, " Cell, vol. 125, no. 4, pp. 775-784, 2006.
13. C. Henneberger, T. Papouin, S. H. R. Oliet, and D. A. Rusakov, "Long-term potentiation depends on release of d-serine from astrocytes, " Nature, vol. 463, no. 7278, pp. 232-236, 2010.
14. P. Fossat, F. R. Turpin, S. Sacchi et al., "Glial D-serine gates NMDA receptors at excitatory synapses in prefrontal cortex, " Cerebral Cortex, vol. 22, no. 3, pp. 595-606, 2012.
15. E. R. Stevens, M. Esguerra, P.M. Kimet al., "D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation ofNMDA receptors, " Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 11, pp. 6789-6794, 2003.
16. E. R. Stevens, E. C. Gustafson, S. J. Sullivan, M. Esguerra, and R. F. Miller, "Light-evoked NMDA receptor-mediated currents are reduced by blocking D-serine synthesis in the salamander retina, " NeuroReport, vol. 21, no. 4, pp. 239-244, 2010.
17. M. Navarrete, G. Perea, D. F. de Sevilla et al., "Astrocytes mediate in vivo cholinergic-induced synaptic plasticity, " PLoS Biology, vol. 10, no. 2, Article ID e1001259, 2012.
18. N. Takata, T. Mishima, C. Hisatsune et al., "Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo, " The Journal of Neuroscience, vol. 31, no. 49, pp. 18155-18165, 2011.
19. N. Chen, H. Sugihara, J. Sharma et al., "Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes, " Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 41, pp. E2832-E2841, 2012.
20. T. A. Fiacco, C. Agulhon, S. R. Taves et al., "Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity, " Neuron, vol. 54, no. 4, pp. 611-626, 2007.
21. D. E. Bonder and K.D. McCarthy, "AstrocyticGq-GPCR-linked IP3R-dependentCa2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo, " Journal of Neuroscience, vol. 34, no. 39, pp. 13139-13150, 2014.
22. K. Nizar, H. Uhlirova, P. Tian et al., "In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase, " Journal of Neuroscience, vol. 33, no. 19, pp. 8411-8422, 2013.
23. J. Petravicz, K. M. Boyt, and K. D. McCarthy, "Astrocyte IP3R2-dependent Ca2+ signaling is not a major modulator of neuronal pathways governing behavior, " Frontiers in Behavioral Neuroscience, vol. 8, article 384, 2014.
24. C. Agulhon, T. A. Fiacco, and K. D. McCarthy, "Hippocampal short-and long-term plasticity are not modulated by astrocyte Ca2+ signaling, " Science, vol. 327, no. 5970, pp. 1250-1254, 2010.
25. M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, "Norepinephrine controls astroglial responsiveness to local circuit activity, " Neuron, vol. 82, no. 6, pp. 1263-1270, 2014.
26. R. E. Paulsen, A. Contestabile, L. Villani, and F. Fonnum, "An in vivo model for studying function of brain tissue temporarily devoid of glial cellmetabolism: the use of fluorocitrate, " Journal of Neurochemistry, vol. 48, no. 5, pp. 1377-1385, 1987.
27. H. Ratiney, Y. Coenradie, S. Cavassila, D. Van Ormondt, and D. Graveron-Demilly, "Time-domain quantitation of 1H short echo-time signals: background accommodation, " Magnetic ResonanceMaterials in Physics: Biology andMedicine, vol. 16, no. 6, pp. 284-296, 2004.
28. K. A. Tennant, D. L. Adkins, N. A. Donlan et al., "The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture, " Cerebral Cortex, vol. 21, no. 4, pp. 865-876, 2011.
29. G. Hess and J. P. Donoghue, "Long-termpotentiation and longterm depression of horizontal connections in rat motor cortex, " Acta Neurobiologiae Experimentalis (Wars), vol. 56, no. 1, pp. 397-405, 1996.
30. T. A. Pologruto, B. L. Sabatini, and K. Svoboda, "ScanImage: flexible software for operating laser scanning microscopes, " BioMedical Engineering Online, vol. 2, article 13, 2003.
31. F. Fonnum, A. Johnsen, and B. Hassel, "Use of fluorocitrate and fluoroacetate in the study of brain metabolism, " Glia, vol. 21, no. 1, pp. 106-113, 1997.
32. X.-Y. Lian and J. L. Stringer, "Inhibition of aconitase in astrocytes increases the sensitivity to chemical convulsants, " Epilepsy Research, vol. 60, no. 1, pp. 41-52, 2004.
33. M. Virgili, R. Paulsen, L. Villani, A. Contestabile, and F. Fonnum, "Temporary impairment ofMuller cell metabolism in the rat retina by intravitreal injection of fluorocitrate, " Experimental Eye Research, vol. 53, no. 1, pp. 115-122, 1991.
34. M. C. McKenna, "The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain, " Journal of Neuroscience Research, vol. 85, no. 15, pp. 3347-3358, 2007.
35. M. Bélanger, I. Allaman, and P. J. Magistretti, "Brain energy metabolism: focus on Astrocyte-neuron metabolic cooperation, " Cell Metabolism, vol. 14, no. 6, pp. 724-738, 2011.
36. M.-S. Rioult-Pedotti, D. Friedman, and J. P. Donoghue, "Learning-induced LTP in neocortex, " Science, vol. 290, no. 5491, pp. 533-536, 2000.
37. R. Malinow and R. C. Malenka, "AMPA receptor trafficking and synaptic plasticity, " Annual Review of Neuroscience, vol. 25, pp. 103-126, 2002.
38. R. Padmashri, B. C. Reiner, A. Suresh, E. Spartz, and A. Dunaevsky, "Altered structural and functional synaptic plasticity with motor skill learning in a mouse model of fragile X syndrome, " Journal of Neuroscience, vol. 33, no. 50, pp. 19715-19723, 2013.
39. C. Frisch, M. Theis, M. A. D. S. Silva et al., "Mice with astrocyte-directed inactivation of connexin43 exhibit increased exploratory behaviour, impaired motor capacities, and changes in brain acetylcholine levels, " European Journal of Neuroscience, vol. 18, no. 8, pp. 2313-2318, 2003.
40. M. M. Halassa, C. Florian, T. Fellin et al., "Astrocyticmodulation of sleep homeostasis and cognitive consequences of sleep loss, " Neuron, vol. 61, no. 2, pp. 213-219, 2009.
41. V. A. Skucas, I. B. Mathews, J. Yang et al., "Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4, " The Journal of Neuroscience, vol. 31, no. 17, pp. 6392-6397, 2011.
42. H. S. Lee, A. Ghetti, A. Pinto-Duarte et al., "Astrocytes contribute to gamma oscillations and recognition memory, " Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 32, pp. E3343-E3352, 2014.
43. A. Suzuki, S. A. Stern, O. Bozdagi et al., "Astrocyte-neuron lactate transport is required for long-term memory formation, " Cell, vol. 144, no. 5, pp. 810-823, 2011.
44. A. Lima, V. M. Sardinha, A. F. Oliveira et al., "Astrocyte pathology in the prefrontal cortex impairs the cognitive function of rats, " Molecular Psychiatry, vol. 19, no. 7, pp. 834-841, 2014.
45. Z. Zhang, N. Gong, W. Wang, L. Xu, and T.-L. Xu, "Bell-shaped D-serine actions on hippocampal long-term depression and spatial memory retrieval, " Cerebral Cortex, vol. 18, no. 10, pp. 2391-2401, 2008.
46. E. Shigetomi, X. Tong, K. Y. Kwan, D. P. Corey, and B. S. Khakh, "TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3, " Nature Neuroscience, vol. 15, no. 1, pp. 70-80, 2012.
47. M. D. Haustein, S. Kracun, X.-H. Lu et al., "Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway, " Neuron, vol. 82, no. 2, pp. 413-429, 2014.
48. K. Kanemaru, H. Sekiya, M. Xu et al., "In vivo visualization of subtle, transient, and local activity of astrocytes using an ultrasensitive Ca2+ indicator, " Cell Reports, vol. 8, no. 1, pp. 311-318, 2014.
49. M. Tanaka, P.-Y. Shih, H. Gomi et al., "Astrocytic Ca2+ signals are required for the functional integrity of tripartite synapses, " Molecular Brain, vol. 6, article 6, 2013.
50. X. Cao, L. P. Li, Q. Wang et al., "Astrocyte-derived ATP modulates depressive-like behaviors, " Nature Medicine, vol. 19, no. 6, pp. 773-777, 2013.
51. B. Hassel, R. E. Paulsen, A. Johnsen, and F. Fonnum, "Selective inhibition of glial cellmetabolism in vivo by fluorocitrate, " Brain Research, vol. 576, no. 1, pp. 120-124, 1992.
52. J. Kur and E. A. Newman, "Purinergic control of vascular tone in the retina, " The Journal of Physiology, vol. 592, part 3, pp. 491-504, 2014.
53. S. Duffy, V. Labrie, and J. C. Roder, "D-serine augmentsNMDANR2B receptor-dependent hippocampal long-term depression and spatial reversal learning, " Neuropsychopharmacology, vol. 33, no. 5, pp. 1004-1018, 2008.
54. P. Bado, C. Madeira, C. Vargas-Lopes et al., "Effects of lowdose d-serine on recognition and working memory in mice, " Psychopharmacology, vol. 218, no. 3, pp. 461-470, 2011.
55. M. Gómez-Galán, D. De Bundel, A. Van Eeckhaut, I. Smolders, and M. Lindskog, "Dysfunctional astrocytic regulation of glutamate transmission in a rat model of depression, " Molecular Psychiatry, vol. 18, no. 5, pp. 582-594, 2013.
56. J. Marchaland, C. Calì, S. M. Voglmaier et al., "Fast subplasma membrane Ca2+ transients control exo-endocytosis of synapticlike microvesicles in astrocytes, " The Journal of Neuroscience, vol. 28, no. 37, pp. 9122-9132, 2008.
57. C. Bonansco, A. Couve, G. Perea, C. Á. Ferradas, M. Roncagliolo, and M. Fuenzalida, "Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity, " European Journal of Neuroscience, vol. 33, no. 8, pp. 1483-1492, 2011.
58. H. W. Kessels and R. Malinow, "Synaptic AMPA receptor plasticity and behavior, " Neuron, vol. 61, no. 3, pp. 340-350, 2009.
59. S. Rumpel, J. LeDoux, A. Zador, and R. Malinow, "Postsynaptic receptor trafficking underlying a form of associative learning, " Science, vol. 308, no. 5718, pp. 83-88, 2005.
60. J. R. Whitlock, A. J. Heynen, M. G. Shuler, and M. F. Bear, "Learning induces long-termpotentiation in the hippocampus, " Science, vol. 313, no. 5790, pp. 1093-1097, 2006.
61. N. Matsuo, L. Reijmers, and M. Mayford, "Spine-type-specific recruitment of newly synthesized AMPA receptors with learning, " Science, vol. 319, no. 5866, pp. 1104-1107, 2008.
62. R. L. Clem and R. L. Huganir, "Calcium-permeable AMPA receptor dynamics mediate fear memory erasure, " Science, vol. 330, no. 6007, pp. 1108-1112, 2010.
63. T. Xu, X. Yu, A. J. Perlik et al., "Rapid formation and selective stabilization of synapses for enduringmotormemories, " Nature, vol. 462, no. 7275, pp. 915-919, 2009.
64. K. J. Harms, M. S. Rioult-Pedotti, D. R. Carter, and A. Dunaevsky, "Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex, " Journal of Neuroscience, vol. 28, no. 22, pp. 5686-5690, 2008.
65. G. Yang, F. Pan, and W. B. Gan, "Stably maintained dendritic spines are associated with lifelong memories, " Nature, vol. 462, no. 7275, pp. 920-924, 2009.
66. Y. Bernardinelli, J. Randall, E. Janett et al., "Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability, " Current Biology, vol. 24, no. 15, pp. 1679-1688, 2014.
67. A. Perez-Alvarez, M. Navarrete, A. Covelo, E. D. Martin, and A. Araque, "Structural and functional plasticity of astrocyte processes and dendritic spine interactions, " Journal ofNeuroscience, vol. 34, no. 38, pp. 12738-12744, 2014.