Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment

Journal of Neuroscience

Volumn 30, Issue 22, 2010, Pages 7507-7515

  Dumitriu, Dani ^a   Hao, Jiandong ^a,b   Hara, Yuko ^a   Kaufmann, Jeffrey ^a   Janssen, William G M ^a   Lou, Wendy ^c   Rapp, Peter R ^d   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b HEBEI MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TORONTO   (Canada)

^d NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DENSITY; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; LEARNING; MALE; MEMORY; MORPHOMETRICS; MUSHROOM; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPINE; SYNAPSE; TASK PERFORMANCE;

AGE FACTORS; AGING; ANIMALS; COGNITION DISORDERS; DENDRITIC SPINES; FEMALE; LINEAR MODELS; MACACA MULATTA; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; REACTION TIME; RECOGNITION (PSYCHOLOGY); SYNAPSES;

EID: 77953189368     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6410-09.2010     Document Type: Article

References (53)

1. Adams MM, Shah RA, Janssen WG, Morrison JH (2001) Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci U S A 98:8071-8076.
2. Bachevalier J, Landis LS, Walker LC, Brickson M, Mishkin M, Price DL, Cork LC (1991) Aged monkeys exhibit behavioral deficits indicative of wide-spread cerebral dysfunction. Neurobiol Aging 12:99-111.
3. Baxter MG, Murray EA (2001) Opposite relationship of hippocampal and rhinal cortex damage to delayed nonmatching-to-sample deficits in monkeys. Hippocampus 11:61-71.
4. Beason-Held LL, Rosene DL, Killiany RJ, Moss MB (1999) Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9:562-574.
5. Bourne J, Harris KM (2007) Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 17:381-386.
6. Bussière T, Gold G, Kövari E, Giannakopoulos P, Bouras C, Perl DP, Morrison JH, Hof PR (2003) Stereologic analysis of neurofibrillary tangle formation in prefrontal cortex area 9 in aging and Alzheimer's disease. Neuroscience 117:577-592. (Pubitemid 36263153)
7. Chang YM, Rosene DL, Killiany RJ, Mangiamele LA, Luebke JI (2005) Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cereb Cortex 15:409-418.
8. Coling D, Kachar B (2001) Theory and application of fluorescence microscopy. Curr Protoc Neurosci 50:2.1.1-2.1.14.
9. de Groot DM, Bierman EP (1986) A critical evaluation of methods for estimating the numerical density of synapses. J Neurosci Methods 18:79-101.
10. Duan H, Wearne SL, Rocher AB, Macedo A, Morrison JH, Hof PR (2003) Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13:950-961. (Pubitemid 37064832)
11. Fuster JM (2008) The prefrontal cortex. San Diego: Elsevier.
12. Gallagher M, Rapp PR (1997) The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339-370. (Pubitemid 127485180)
13. Goldman-Rakic PS (2002) The "psychic cell" of Ramón y Cajal. Prog Brain Res 136:427-434.
14. Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812-816. (Pubitemid 36019628)
15. Hao J, Rapp PR, Leffler AE, Leffler SR, Janssen WG, Lou W, McKay H, Roberts JA, Wearne SL, Hof PR, Morrison JH (2006) Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 26:2571-2578. (Pubitemid 44699017)
16. Hao J, Rapp PR, Janssen WG, Lou W, Lasley BL, Hof PR, Morrison JH (2007) Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci U S A 104:11465-11470. (Pubitemid 47175163)
17. Harris KM, Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
18. Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685-2705.
19. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441:979-983. (Pubitemid 43980351)
20. Horton S, Baker J, Schorer J (2008) Expertise and aging: maintaining skills through the lifespan. Eur Rev Aging Phys Act 5:89-96.
21. Jones EG (1984) Laminar distribution of cortical efferent cells. In: Cerebral cortex, Vol 1, Cellular components of the cerebral cortex (Peters A, Jones EG, eds), pp 521-553. New York: Plenum.
22. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26:360-368.
23. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129.
24. Kopec C, Malinow R (2006) Neuroscience. Matters of size. Science 314:1554-1555.
25. Kramer AF, Bherer L, Colcombe SJ, Dong W, Greenough WT (2004) Environmental influences on cognitive and brain plasticity during aging. J Gerontol A Biol Sci Med Sci 59:M940-57.
26. Makris N, Papadimitriou GM, van der Kouwe A, Kennedy DN, Hodge SM, Dale AM, Benner T, Wald LL, Wu O, Tuch DS, Caviness VS, Moore TL, Killiany RJ, Moss MB, Rosene DL (2007) Frontal connections and cognitive changes in normal aging rhesus monkeys: A DTI study. Neurobiol Aging 28:1556-1567.
27. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
28. Miller EK, Freedman DJ, Wallis JD (2002) The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci 357:1123-1136. (Pubitemid 34973722)
29. Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412-419.
30. Moss MB, Killiany RJ, Herndon JG (1999) Age-related cognitive decline in rhesus monkey. In: Cerebral cortex, neurodegenerative and age-related changes in structure and function of cerebral cortex (Peters A, Morrison JH, eds), pp 21-48. New York: Kluwer Academic/Plenum.
31. Murray EA, Mishkin M (1998) Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18:6568-6582.
32. O'Donnell KA, Rapp PR, Hof PR (1999) Preservation of prefrontal cortical volume in behaviorally characterized aged macaque monkeys. Exp Neurol 160:300-310.
33. Peters A, Rosene DL (2003) In aging, is it gray or white? J Comp Neurol 462:139-143.
34. Peters A, Sethares C (2002) Aging and the myelinated fibers in prefrontal cortex and corpus callosum of the monkey. J Comp Neurol 442:277-291. (Pubitemid 34024374)
35. Peters A, Morrison JH, Rosene DL, Hyman BT (1998a) Feature article: are neurons lost from the primate cerebral cortex during normal aging? Cereb Cortex 8:295-300.
36. Peters A, Sethares C, Moss MB (1998b) The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. Cereb Cortex 8:671-684. (Pubitemid 28550890)
37. Peters A, Sethares C, Luebke JI (2008) Synapses are lost during aging in the primate prefrontal cortex. Neuroscience 152:970-981.
38. Rapp PR, Amaral DG (1989) Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 9:3568-3576.
39. Rapp PR, Amaral DG (1991) Recognition memory deficits in a subpopulation of aged monkeys resemble the effects of medial temporal lobe damage. Neurobiol Aging 12:481-486.
40. Rapp PR, Morrison JH, Roberts JA (2003) Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 23:5708-5714.
41. 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 1:2152-2161. (Pubitemid 46773338)
42. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL (2008) Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3:e1997.
43. Shamy JL, Barnes CA, Amaral DG, Buonocore MH, Hof PR, Rapp PR (2006a) Regional volumetric correlates of spatiotemporal and recognition memory impairment in aged rhesus monkeys. Soc Neurosci Abstr 32:371.15.
44. Shamy JL, Buonocore MH, Makaron LM, Amaral DG, Barnes CA, Rapp PR (2006b) Hippocampal volume is preserved and fails to predict recognition memory impairment in aged rhesus monkeys (Macaca mulatta). Neurobiol Aging 27:1405-1415.
45. Sorra KE, Harris KM (2000) Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10:501-511.
46. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127-136.
47. Takumi Y, Ramírez-León V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
48. Tigges J, Herndon JG, Rosene DL (1996) Preservation into old age of synaptic number and size in the supragranular layer of the dentate gyrus in rhesus monkeys. Acta Anat (Basel) 157:63-72.
49. Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920-924.
50. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H (2008) Principles of long-term dynamics of dendritic spines. J Neurosci 28:13592-13608.
51. Zola SM, Squire LR (2001) Relationship between magnitude of damage to the hippocampus and impaired recognition memory in monkeys. Hippocampus 11:92-98.
52. Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451-463.
53. Zuo Y, Lin A, Chang P, Gan WB (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181-189.