Short-term sleep deprivation disrupts the molecular composition of ionotropic glutamate receptors in entorhinal cortex and impairs the rat spatial reference memory

Behavioural Brain Research

Volumn 300, Issue , 2016, Pages 70-76

  Xie, Meilan ^a   Li, Chao ^a   He, Chao ^a   Yang, Li ^a   Tan, Gang ^a   Yan, Jie ^a   Wang, Jiali ^a   Hu, Zhian ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Entorhinal cortex; Ionotropic glutamate receptor; Morris water maze; Sleep deprivation

Indexed keywords

AMPA RECEPTOR; GLUA1 PROTEIN; GLUA2 PROTEIN; GLUA3 PROTEIN; GLUN1 PROTEIN; IONOTROPIC RECEPTOR; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE; GLUN1 GENE; GLUN2A GENE; GLUN2B GENE; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL PERFORMANCE; MORRIS WATER MAZE TEST; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REFERENCE MEMORY; SLEEP DEPRIVATION; SPATIAL MEMORY; ANIMAL; BIOTINYLATION; DISEASE MODEL; EMOTION; ENTORHINAL CORTEX; MAZE TEST; MEMORY DISORDERS; METABOLISM; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; EMOTIONS; ENTORHINAL CORTEX; MALE; MAZE LEARNING; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TESTS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SLEEP DEPRIVATION; SPATIAL MEMORY;

EID: 84949921749     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.10.002     Document Type: Article

References (54)

1. Xie L., Kang H., Xu Q., Chen M.J., Liao Y., Thiyagarajan M., et al. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377.
2. Yang G., Lai C.S., Cichon J., Ma L., Li W., Gan W.B. Sleep promotes branch-specific formation of dendritic spines after learning. Science 2014, 344:1173-1178.
3. Oudiette D., Antony J.W., Creery J.D., Paller K.A. The role of memory reactivation during wakefulness and sleep in determining which memories endure. J. Neurosci. 2013, 33:6672-6678.
4. Shen J., Kudrimoti H.S., McNaughton B.L., Barnes C.A. Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience. J. Sleep Res. 1998, 7(Suppl. 1):6-16.
5. Paller K.A., Voss J.L. Memory reactivation and consolidation during sleep. Learn. Mem. 2004, 11:664-670.
6. Yan J., Li J.C., Xie M.L., Zhang D., Qi A.P., Hu B., et al. Short-term sleep deprivation increases intrinsic excitability of prefrontal cortical neurons. Brain Res. 2011, 1401:52-58.
7. Wang G.P., Huang L.Q., Wu H.J., Zhang L., You Z.D., Zhao Z.X. Calcineurin contributes to spatial memory impairment induced by rapid eye movement sleep deprivation. Neuroreport 2009, 20:1172-1176.
8. Li S., Tian Y., Ding Y., Jin X., Yan C., Shen X. The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats. Learn. Behav. 2009, 37:246-253.
9. Guan Z., Peng X., Fang J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res. 2004, 1018:38-47.
10. Dorokhov V.B., Kozhedub R.G., Arsen'ev G.N., Kozhechkin S.N., Ukraintseva Iu V., Kulikov M.A., et al. [Sleep deprivation effect upon spatial memory consolidation in rats after one-day learning in a morris water maze]. Zh. Vses. Nerv. Deyat. 2011, 61:322-331.
11. Zhao Z., Li Y., Chen H., Huang L., Zhao F., Yu Q., et al. Xylaria nigripes mitigates spatial memory impairment induced by rapid eye movement sleep deprivation. Int. J. Clin. Exp. Med. 2014, 7:356-362.
12. Alzoubi K.H., Khabour O.F., Salah H.A., Abu R., Abu Rashid B.E. The combined effect of sleep deprivation and Western diet on spatial learning and memory: role of BDNF and oxidative stress. J. Mol. Neurosci. 2013, 50:124-133.
13. Xie M., Yan J., He C., Yang L., Tan G., Li C., et al. Short-term sleep deprivation impairs spatial working memory and modulates expression levels of ionotropic glutamate receptor subunits in hippocampus. Behav. Brain Res. 2015, 286:64-70.
14. Hagewoud R., Havekes R., Novati A., Keijser J.N., Van der Zee E.A., Meerlo P. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J. Sleep Res. 2010, 19:280-288.
15. Deng P.Y., Xiao Z., Yang C., Rojanathammanee L., Grisanti L., Watt J., et al. GABA(B) receptor activation inhibits neuronal excitability and spatial learning in the entorhinal cortex by activating TREK-2 K+ channels. Neuron 2009, 63:230-243.
16. Steffenach H.A., Witter M., Moser M.B., Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 2005, 45:301-313.
17. Van Cauter T., Camon J., Alvernh A., Elduayen C., Sargolini F., Save E. Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb. Cortex 2013, 23:451-459.
18. Canto C.B., Wouterlood F.G., Witter M.P. What does the anatomical organization of the entorhinal cortex tell us?. Neural Plast. 2008, 2008:381243.
19. van Strien N.M., Cappaert N.L., Witter M.P. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 2009, 10:272-282.
20. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.B., et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
21. Ray S., Naumann R., Burgalossi A., Tang Q., Schmidt H., Brecht M. Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 2014, 343:891-896.
22. Fyhn M., Molden S., Witter M.P., Moser E.I., Moser M.B. Spatial representation in the entorhinal cortex. Science 2004, 305:1258-1264.
23. Nunes G.P., Tufik S., Nobrega J.N. Decreased muscarinic receptor binding in rat brain after paradoxical sleep deprivation: an autoradiographic study. Brain Res. 1994, 645:247-252.
24. Nunes G.P., Tufik S., Nobrega J.N. Autoradiographic analysis of D1 and D2 dopaminergic receptors in rat brain after paradoxical sleep deprivation. Brain Res. Bull. 1994, 34:453-456.
25. Wollmuth L.P., Sobolevsky A.I. Structure and gating of the glutamate receptor ion channel. Trends Neurosci. 2004, 27:321-328.
26. Davis S., Butcher S.P., Morris R.G. The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J. Neurosci. 1992, 12:21-34.
27. Allen K., Gil M., Resnik E., Toader O., Seeburg P., Monyer H. Impaired path integration and grid cell spatial periodicity in mice lacking GluA1-containing AMPA receptors. J. Neurosci. 2014, 34:6245-6259.
28. Sanderson D.J., Gray A., Simon A., Taylor A.M., Deacon R.M., Seeburg P.H., et al. Deletion of glutamate receptor-A (GluR-A) AMPA receptor subunits impairs one-trial spatial memory. Behav. Neurosci. 2007, 121:559-569.
29. Ravassard P., Pachoud B., Comte J.C., Mejia-Perez C., Scote-Blachon C., Gay N., et al. Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. Sleep 2009, 32:227-240.
30. Lopez J., Roffwarg H.P., Dreher A., Bissette G., Karolewicz B., Shaffery J.P. Rapid eye movement sleep deprivation decreases long-term potentiation stability and affects some glutamatergic signaling proteins during hippocampal development. Neuroscience 2008, 153:44-53.
31. Kopp C., Longordo F., Nicholson J.R., Luthi A. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J. Neurosci. 2006, 26:12456-12465.
32. Vecsey C.G., Baillie G.S., Jaganath D., Havekes R., Daniels A., Wimmer M., et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 2009, 461:1122-1125.
33. Isaac J.T., Ashby M.C., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
34. Blahos J., Wenthold R.J. Relationship between N-methyl-d-aspartate receptor NR1 splice variants and NR2 subunits. J. Biol. Chem. 1996, 271:15669-15674.
35. He C., Luo F., Chen X., Chen F., Li C., Ren S., et al. Superficial layer-specific histaminergic modulation of medial entorhinal cortex required for spatial learning. Cereb. Cortex 2015, Online (bhu322).
36. Li Y., Fan S., Yan J., Li B., Chen F., Xia J., et al. Adenosine modulates the excitability of layer II stellate neurons in entorhinal cortex through A1 receptors. Hippocampus 2011, 21:265-280.
37. Diering G.H., Gustina A.S., Huganir R.L. PKA-GluA1 coupling via AKAP5 controls AMPA receptor phosphorylation and cell-surface targeting during bidirectional homeostatic plasticity. Neuron 2014, 84:790-805.
38. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Ann. Rev. Neurosci. 2008, 31:69-89.
39. Olson V.G., Zabetian C.P., Bolanos C.A., Edwards S., Barrot M., Eisch A.J., et al. Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J. Neurosci. 2005, 25:5553-5562.
40. Guzman-Marin R., Ying Z., Suntsova N., Methippara M., Bashir T., Szymusiak R., et al. Suppression of hippocampal plasticity-related gene expression by sleep deprivation in rats. J. Physiol. 2006, 575:807-819.
41. Acosta-Pena E., Camacho-Abrego I., Melgarejo-Gutierrez M., Flores G., Drucker-Colin R., Garcia-Garcia F. Sleep deprivation induces differential morphological changes in the hippocampus and prefrontal cortex in young and old rats. Synapse 2015, 69:15-25.
42. Guzman-Marin R., Suntsova N., Stewart D.R., Gong H., Szymusiak R., McGinty D. Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J. Physiol. 2003, 549:563-571.
43. Mueller A.D., Parfyonov M., Pavlovski I., Marchant E.G., Mistlberger R.E. The inhibitory effect of sleep deprivation on cell proliferation in the hippocampus of adult mice is eliminated by corticosterone clamp combined with interleukin-1 receptor 1 knockout. Brain Behav. Immun. 2014, 35:182-188.
44. Sanderson D.J., Bannerman D.M. The role of habituation in hippocampus-dependent spatial working memory tasks: evidence from GluA1 AMPA receptor subunit knockout mice. Hippocampus 2012, 22:981-994.
45. Sanderson D.J., Good M.A., Skelton K., Sprengel R., Seeburg P.H., Rawlins J.N., et al. Enhanced long-term and impaired short-term spatial memory in GluA1 AMPA receptor subunit knockout mice: evidence for a dual-process memory model. Learn. Mem. 2009, 16:379-386.
46. Sanderson D.J., Sprengel R., Seeburg P.H., Bannerman D.M. Deletion of the GluA1 AMPA receptor subunit alters the expression of short-term memory. Learn. Mem. 2011, 18:128-131.
47. Chen C., Hardy M., Zhang J., LaHoste G.J., Bazan N.G. Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments. Biochem. Biophys. Res. Commun. 2006, 340:435-440.
48. Park H.J., Kang W.S., Paik J.W., Kim J.W. Effect of valproic acid through regulation of NMDA receptor-ERK signaling in sleep deprivation rats. J. Mol. Neurosci. 2012, 47:554-558.
49. Kim E., Grover L.M., Bertolotti D., Green T.L. Growth hormone rescues hippocampal synaptic function after sleep deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1588-R1596.
50. McDermott C.M., Hardy M.N., Bazan N.G., Magee J.C. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J. Physiol. 2006, 570:553-565.
51. McDermott C.M., LaHoste G.J., Chen C., Musto A., Bazan N.G., Magee J.C. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J. Neurosci. 2003, 23:9687-9695.
52. Van Cauter T., Poucet B., Save E. Unstable CA1 place cell representation in rats with entorhinal cortex lesions European. J. Neurosci. 2008, 27:1933-1946.
53. Bush D., Barry C., Burgess N. What do grid cells contribute to place cell firing?. Trends Neurosci. 2014, 37:136-145.
54. Barria A., Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 2005, 48:289-301.