Glutamatergic regulation prevents hippocampal-dependent age-related cognitive decline through dendritic spine clustering

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

Volumn 111, Issue 52, 2014, Pages 18733-18738

  Pereira, Ana C ^a   Lambert, Hilary K ^a   Grossman, Yael S ^b   Dumitriu, Dani ^b   Waldman, Rachel ^b   Jannetty, Sophia K ^a   Calakos, Katina ^a   Janssen, William G ^b   McEwen, Bruce S ^a   Morrison, John H ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cognitive aging; Dendritic spine clustering; Glutamate; Neuroplasticity; Riluzole

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RILUZOLE; NEUROPROTECTIVE AGENT;

AGED; AGING; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; COGNITIVE DEFECT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DEMENTIA; DENDRITIC SPINE; HIPPOCAMPUS; MAZE TEST; MEMORY; MENTAL DETERIORATION; MORPHOLOGY; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; ANIMAL; DENDRITE; DRUG EFFECTS; HIPPOCAMPAL CA1 REGION; MALE; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

ANIMALIA; BASIDIOMYCOTA; RATTUS;

AGING; ANIMALS; CA1 REGION, HIPPOCAMPAL; COGNITION; DENDRITES; GLUTAMIC ACID; MALE; MEMORY; NEUROPROTECTIVE AGENTS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RILUZOLE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84924543911     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421285111     Document Type: Article

References (50)

1. Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7(1):30-40.
2. Morrison JH, Baxter MG (2012) The ageing cortical synapse: Hallmarks and implications for cognitive decline. Nat Rev Neurosci 13(4):240-250.
3. Buckner RL (2004) Memory and executive function in aging and AD: Multiple factors that cause decline and reserve factors that compensate. Neuron 44(1):195-208.
4. Barnes CA (1979) Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93(1):74-104.
5. Dumitriu D, et al. (2010) Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 30(22):7507-7515.
6. Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278(5337):412-419.
7. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10(9):647-658.
8. von Bohlen und Halbach O, Zacher C, Gass P, Unsicker K (2006) Age-related alterations in hippocampal spines and deficiencies in spatial memory in mice. J Neurosci Res 83(4):525-531.
9. deToledo-Morrell L, Geinisman Y, Morrell F (1988) Age-dependent alterations in hippocampal synaptic plasticity: Relation to memory disorders. Neurobiol Aging 9(5-6):581-590.
10. Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420(6917):812-816.
11. Trachtenberg JT, et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420(6917):788-794.
12. Hardingham GE (2006) Pro-survival signalling from the NMDA receptor. Biochem Soc Trans 34(Pt 5):936-938.
13. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: Implications for neurodegenerative disorders. Nat Rev Neurosci 11(10):682-696.
14. Potier B, et al. (2010) Reduction in glutamate uptake is associated with extrasynaptic NMDA and metabotropic glutamate receptor activation at the hippocampal CA1 synapse of aged rats. Aging Cell 9(5):722-735.
15. Brothers HM, et al. (2013) Riluzole partially rescues age-associated, but not LPS-induced, loss of glutamate transporters and spatial memory. J Neuroimmune Pharmacol 8(5):1098-1105.
16. Wheeler DD, Ondo JG (1986) Time course of the aging of the high affinity L-glutamate transporter in rat cortical synaptosomes. Exp Gerontol 21(3):159-168.
17. Vatassery GT, Lai JC, Smith WE, Quach HT (1998) Aging is associated with a decrease in synaptosomal glutamate uptake and an increase in the susceptibility of synaptosomal vitamin E to oxidative stress. Neurochem Res 23(2):121-125.
18. Martin D, Thompson MA, Nadler JV (1993) The neuroprotective agent riluzole inhibits release of glutamate and aspartate from slices of hippocampal area CA1. Eur J Pharmacol 250(3):473-476.
19. Fumagalli E, Funicello M, Rauen T, Gobbi M, Mennini T (2008) Riluzole enhances the activity of glutamate transporters GLAST, GLT1 and EAAC1. Eur J Pharmacol 578(2-3):171-176.
20. Frizzo ME, Dall'Onder LP, Dalcin KB, Souza DO (2004) Riluzole enhances glutamate uptake in rat astrocyte cultures. Cell Mol Neurobiol 24(1):123-128.
21. Banasr M, et al. (2010) Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry 15(5):501-511.
22. Chowdhury GM, et al. (2008) Chronic riluzole treatment increases glucose metabolism in rat prefrontal cortex and hippocampus. J Cereb Blood Flow Metab 28(12):1892-1897.
23. Brennan BP, et al. (2010) Rapid enhancement of glutamatergic neurotransmission in bipolar depression following treatment with riluzole. Neuropsychopharmacology 35(3):834-846.
24. Mu X, Azbill RD, Springer JE (2000) Riluzole improves measures of oxidative stress following traumatic spinal cord injury. Brain Res 870(1-2):66-72.
25. Mizuta I, et al. (2001) Riluzole stimulates nerve growth factor, brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor synthesis in cultured mouse astrocytes. Neurosci Lett 310(2-3):117-120.
26. Polsky A, Mel BW, Schiller J (2004) Computational subunits in thin dendrites of pyramidal cells. Nat Neurosci 7(6):621-627.
27. Larkum ME, Nevian T (2008) Synaptic clustering by dendritic signalling mechanisms. Curr Opin Neurobiol 18(3):321-331.
28. Kleindienst T, Winnubst J, Roth-Alpermann C, Bonhoeffer T, Lohmann C (2011) Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron 72(6):1012-1024.
29. Kavalali ET, Klingauf J, Tsien RW (1999) Activity-dependent regulation of synaptic clustering in a hippocampal culture system. Proc Natl Acad Sci USA 96(22):12893-12900.
30. Bloss EB, et al. (2011) Evidence for reduced experience-dependent dendritic spine plasticity in the aging prefrontal cortex. J Neurosci 31(21):7831-7839.
31. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H (1992) A two-trial memory task with automated recording: Study in young and aged rats. Brain Res 588(1):132-139.
32. Conrad CD, Galea LA, Kuroda Y, McEwen BS (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110(6):1321-1334.
33. Poirazi P, Mel BW (2001) Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29(3):779-796.
34. Harvey CD, Svoboda K (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450(7173):1195-1200.
35. De Roo M, Klauser P, Muller D (2008) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6(9):e219.
36. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375(6530):400-404.
37. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26(7):360-368.
38. Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7(7):575-583.
39. Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105(3):417-537.
40. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6(4):277-284.
41. Goldin M, Segal M, Avignone E (2001) Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J Neurosci 21(1):186-193.
42. Bourne J, Harris KM (2007) Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 17(3):381-386.
43. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441(7096):979-983.
44. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399(6731):66-70.
45. Bourne JN, Harris KM (2011) Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21(4):354-373.
46. Xu T, et al. (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462(7275):915-919.
47. Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462(7275):920-924.
48. Caroni P, Donato F, Muller D (2012) Structural plasticity upon learning: Regulation and functions. Nat Rev Neurosci 13(7):478-490.
49. Rodriguez A, Ehlenberger DB, Hof PR, Wearne SL (2006) Rayburst sampling, an algorithm for automated three-dimensional shape analysis from laser scanning microscopy images. Nat Protoc 1(4):2152-2161.
50. Wearne SL, et al. (2005) New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales. Neuroscience 136(3):661-680.