Cognitive deficits, changes in synaptic function, and brain pathology in a mouse model of normal aging

eNeuro

Volumn 2, Issue 5, 2015, Pages

  Weber, Martin ^a,b   Wu, Tiffany ^a   Hanson, Jesse E ^a   Alam, Nazia M ^c   Solanoy, Hilda ^a   Ngu, Hai ^a   Lauffer, Benjamin E ^a   Lin, Han H ^a   Dominguez, Sara L ^a   Reeder, Jens ^a   Tom, Jennifer ^a   Steiner, Pascal ^a   Foreman, Oded ^a   Prusky, Glen T ^c   Levie, Kimberly Scearce ^a  

^a GENENTECH INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BURKE MEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Age; C Fos; Cognition; Gliosis; Mice; Synaptic function

Indexed keywords

EID: 85014958478     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0047-15.2015     Document Type: Article

References (67)

1. Asztely F, Xiao MY, Gustafsson B (1996) Long-term potentiation and paired-pulse facilitation in the hippocampal CA1 region. Neuroreport 7:1609-1612. Medline
2. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, Mansuy I, Hawkins RD, Kandel ER (1999) Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci U S A 96:5280-5285. Medline
3. Baltes PB, Lindenberger U (1997) Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? Psychol Aging 12:12-21. Medline
4. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93:74-104. Medline
5. Barnes CA, Rao G, McNaughton BL (1996) Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats. Learn Mem 3:124-137. Medline
6. Barrientos RM, Kitt MM, Watkins LR, Maier SF (2015) Neuroinflammation in the normal aging hippocampus. Neuroscience. Advance online publication. Retrieved 5 October 2015. doi:10.1016/j.neuroscience.2015.03.007.
7. Bryan KJ, Lee H, Perry G, Smith MA, Casadesus G (2009) Transgenic mouse models of Alzheimer’s disease: behavioral testing and considerations. In: Methods of behavior analysis in neuroscience (Buccafusco JJ, ed), pp 1-18. Boca Raton: CRC.
8. Burke SN, Ryan L, Barnes CA (2012) Characterizing cognitive aging of recognition memory and related processes in animal models and in humans. Front Aging Neurosci 4:15. CrossRef Medline
9. Carrié I, Debray M, Bourre JM, Francès H (1999) Age-induced cognitive alterations in OF1 mice. Physiol Behav 66:651-656. Medline
10. Caserta MT, Bannon Y, Fernandez F, Giunta B, Schoenberg MR, Tan J (2009) Normal brain aging clinical, immunological, neuropsychological, and neuroimaging features. Int Rev Neurobiol 84:1-19. CrossRef Medline
11. Cheng XR, Zhou WX, Zhang YX (2014) The behavioral, pathological and therapeutic features of the senescence-accelerated mouse prone 8 strain as an Alzheimer’s disease animal model. Ageing Res Rev 13:13-37. CrossRef Medline
12. Clark MG, Vasilevsky S, Myers TM (2003) Air and shock two-way shuttlebox avoidance in C57BL/6J and 129X1/SvJ mice. Physiol Behav 78:117-123. Medline
13. Crawley JN (2007) What’s wrong with my mouse: behavioral phenotyping of transgenic and knockout mice. Hoboken: Wiley.
14. Deupree DL, Bradley J, Turner DA (1993) Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol Aging 14: 249-258. Medline
15. Dolgin E (2013) Old mice require new experimental tricks to study aging process. Nat Med 19:518-519. CrossRef Medline
16. Douglas RM, Alam NM, Silver BD, McGill TJ, Tschetter WW, Prusky GT (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci 22:677-684. CrossRef Medline
17. Durkin M, Prescott L, Furchtgott E, Cantor J, Powell DA (1993) Concomitant eyeblink and heart rate classical conditioning in young, middle-aged, and elderly human subjects. Psychol Aging 8:571-581. Medline
18. Erickson CA, Barnes CA (2003) The neurobiology of memory changes in normal aging. Exp Gerontol 38:61-69. Medline
19. Farso M, Menard C, Colby-Milley J, Quirion R (2013) Immune marker CD68 correlates with cognitive impairment in normally aged rats. Neurobiol Aging 34:1971-1976. CrossRef Medline
20. Foldi CJ, Eyles DW, McGrath JJ, Burne TH (2011) The effects of breeding protocol in C57BL/6J mice on adult offspring behaviour. PLoS One 6:e18152. CrossRef Medline
21. Francis HW, Ryugo DK, Gorelikow MJ, Prosen CA, May BJ (2003) The functional age of hearing loss in a mouse model of presbycusis. II. Neuroanatomical correlates. Hear Res 183:29-36. Medline
22. Geldmacher DS, Levin BE, Wright CB (2012) Characterizing healthy samples for studies of human cognitive aging. Front Aging Neurosci 4:23. CrossRef Medline
23. Glisky EL (2007) Changes in Cognitive Function in Human Aging. In: Brain aging: models, methods, and mechanisms (Riddle DR, ed). Boca Raton, FL: CRC.
24. Hanson JE, Meilandt WJ, Gogineni A, Reynen P, Herrington J, Weimer RM, Scearce-Levie K, Zhou Q (2014) Chronic GluN2B antagonism disrupts behavior in wild-type mice without protecting against synapse loss or memory impairment in Alzheimer’s disease mouse models. J Neurosci 34:8277-8288. CrossRef Medline
25. Ison JR, Allen PD, O’Neill WE (2007) Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequencyspecific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex. J Assoc Res Otolaryngol 8:539-550. CrossRef Medline
26. Johnson KR, Erway LC, Cook SA, Willott JF, Zheng QY (1997) A major gene affecting age-related hearing loss in C57BL/6J mice. Hear Res 114:83-92. Medline
27. Kennard JA, Woodruff-Pak DS (2011) Age sensitivity of behavioral tests and brain substrates of normal aging in mice. Front Aging Neurosci 3:9. CrossRef Medline
28. King DL, Arendash GW (2002) Behavioral characterization of the Tg2576 transgenic model of Alzheimer’s disease through 19 months. Physiol Behav 75:627-642. Medline
29. Kumar A, Foster TC (2013) Linking redox regulation of NMDAR synaptic function to cognitive decline during aging. J Neurosci 33:15710-15715. CrossRef Medline
30. Lee YI, Park KH, Baik SH, Cha CI (1998) Attenuation of c-Fos basal expression in the cerebral cortex of aged rat. Neuroreport 9:2733-2736. Medline
31. Li HS, Borg E (1991) Age-related loss of auditory sensitivity in two mouse genotypes. Acta Otolaryngol 111:827-834. Medline
32. Lithfous S, Dufour A, Després O (2013) Spatial navigation in normal aging and the prodromal stage of Alzheimer’s disease: insights from imaging and behavioral studies. Ageing Res Rev 12:201-213. CrossRef Medline
33. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87-136. CrossRef Medline
34. Martin del Campo HN, Measor KR, Razak KA (2012) Parvalbumin immunoreactivity in the auditory cortex of a mouse model of presbycusis. Hear Res 294:31-39. CrossRef Medline
35. Miyamoto E (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100:433-442. Medline
36. Moffat SD, Resnick SM (2002) Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behav Neurosci 116:851-859. Medline
37. Murray EA, Bussey TJ (1999) Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn Sci 3:142-151. Medline
38. Newton JR, Ellsworth C, Miyakawa T, Tonegawa S, Sur M (2004) Acceleration of visually cued conditioned fear through the auditory pathway. Nat Neurosci 7:968-973. CrossRef Medline
39. Norris CM, Korol DL, Foster TC (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 16:5382-5392. Medline
40. Norris CM, Halpain S, Foster TC (1998) Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 80:1567-1570. Medline
41. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J Neurosci 26:10129-10140. CrossRef Medline
42. Oliverio A, Eleftheriou BE, Bailey DW (1973) A gene influencing active avoidance performance in mice. Physiol Behav 11:497-501. Medline
43. Ouagazzal AM, Reiss D, Romand R (2006) Effects of age-related hearing loss on startle reflex and prepulse inhibition in mice on pure and mixed C57BL and 129 genetic background. Behav Brain Res 172:307-315. CrossRef Medline
44. Palop JJ, Chin J, Bien-Ly N, Massaro C, Yeung BZ, Yu GQ, Mucke L (2005) Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 25:9686-9693. CrossRef Medline
45. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer’s disease-related cognitive deficits. Proc Natl Acad Sci U S A 100:9572-9577. CrossRef Medline
46. Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP (2013) The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement 9:63-75.e2. CrossRef Medline
47. Prusky GT, Alam NM, Douglas RM (2006) Enhancement of vision by monocular deprivation in adult mice. J Neurosci 26:11554-11561. CrossRef Medline
48. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45:4611-4616. CrossRef Medline
49. Rodríguez-Arellano JJ, Parpura V, Zorec R, Verkhratsky A (2015) Astrocytes in physiological aging and Alzheimer’s disease. Neuroscience. Advance online publication. Retrieved 5 October 2015. CrossRef Medline
50. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179. Medline
51. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA (1997) Role of temporal summation in age-related long-term potentiationinduction deficits. Hippocampus 7:549-558. CrossRef Medline
52. Schulz PE, Cook EP, Johnston D (1994) Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J Neurosci 14:5325-5337. Medline
53. Solomon PR, Blanchard S, Levine E, Velazquez E, Groccia-Ellison M (1991) Attenuation of age-related conditioning deficits in humans by extension of the interstimulus interval. Psychol Aging 6:36-42. Medline
54. Solomon PR, Brett M, Groccia-Ellison ME, Oyler C, Tomasi M, Pendlebury WW (1995) Classical conditioning in patients with Alzheimer’s disease: a multiday study. Psychol Aging 10:248-254. Medline
55. Sparkman NL, Kohman RA, Garcia AK, Boehm GW (2005) Peripheral lipopolysaccharide administration impairs two-way active avoidance conditioning in C57BL/6J mice. Physiol Behav 85:278-288. CrossRef Medline
56. Stuchlik A (2014) Dynamic learning and memory, synaptic plasticity and neurogenesis: an update. Front Behav Neurosci 8:106. Cross-Ref Medline
57. Takahashi T, Amano N, Asamura H, Nomiyama T, Hanihara T, Nakayama J, Fukushima H (2006) Correlation between glial fibrillary acidic protein-positive astrocytes and age in the human hippocampus. Leg Med (Tokyo) 8:161-165. CrossRef Medline
58. Vieira RT, Caixeta L, Machado S, Silva AC, Nardi AE, Arias-Carrión O, Carta MG (2013) Epidemiology of early-onset dementia: a review of the literature. Clin Pract Epidemiol Ment Health 9:88-95. CrossRef Medline
59. Webster SJ, Bachstetter AD, Nelson PT, Schmitt FA, Van Eldik LJ (2014) Using mice to model Alzheimer’s dementia: an overview of the clinical disease and the preclinical behavioral changes in 10 mouse models. Front Genet 5:88. CrossRef Medline
60. Wood KM, Edwards JD, Clay OJ, Wadley VG, Roenker DL, Ball KK (2005) Sensory and cognitive factors influencing functional ability in older adults. Gerontology 51:131-141. CrossRef Medline
61. Woodruff-Pak DS (2001) Eyeblink classical conditioning differentiates normal aging from Alzheimer’s disease. Integr Physiol Behav Sci 36:87-108. Medline
62. Woodruff-Pak DS, Romano S, Papka M (1996a) Training to criterion in eyeblink classical conditioning in Alzheimer’s disease, Down’s syndrome with Alzheimer’s disease, and healthy elderly. Behav Neurosci 110:22-29. Medline
63. Woodruff-Pak DS, Papka M, Romano S, Li YT (1996b) Eyeblink classical conditioning in Alzheimer’s disease and cerebrovascular dementia. Neurobiol Aging 17:505-512. Medline
64. Wright AL, Zinn R, Hohensinn B, Konen LM, Beynon SB, Tan RP, Clark IA, Abdipranoto A, Vissel B (2013) Neuroinflammation and neuronal loss precede Aβ plaque deposition in the hAPP-J20 mouse model of Alzheimer’s disease. PLoS One 8:e59586. Cross-Ref Medline
65. Wu L, Rosa-Neto P, Hsiung GY, Sadovnick AD, Masellis M, Black SE, Jia J, Gauthier S (2012) Early-onset familial Alzheimer’s disease (EOFAD). Can J Neurol Sci 39:436-445. Medline
66. Wyss-Coray T (2006) Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 12:1005-1015. CrossRef Medline
67. Young JW, Wallace CK, Geyer MA, Risbrough VB (2010) Ageassociated improvements in cross-modal prepulse inhibition in mice. Behav Neurosci 124:133-140. CrossRef Medline