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Studying the Impact of Aging on Memory Systems: Contribution of Two Behavioral Models in the Mouse

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Book cover Behavioral Neurobiology of Aging

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 10))

Abstract

In the present chapter, we describe our own attempts to improve our understanding of the pathophysiology of memory in aging. First, we tried to improve animal models of memory degradations occurring in aging, and develop common behavioral tools between mice and humans. Second, we began to use these behavioral tools to identify the molecular/intracellular changes occurring within the integrate network of memory systems in order to bridge the gap between the molecular and system level of analysis. The chapter is divided into three parts (i) modeling aging-related degradation in declarative memory (DM) in mice, (ii) assessing the main components of working memory (WM) with a common radial-maze task in mice and humans and (iii) studying the role of the retinoid cellular signaling path in aging-related changes in memory systems.

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References

  • Addis DR, McAndrews MP (2006) Prefrontal and hippocampal contributions to the generation and binding of semantic associations during successful encoding. Neuroimage 33:1194–1206

    Article  PubMed  Google Scholar 

  • Baddeley A (1996) The fractionation of working memory. Proc Natl Acad Sci U S A 93:13468–13472

    Article  PubMed  CAS  Google Scholar 

  • Baddeley A, Cocchini G, Della Sala S, Logie RH, Spinnler H (1999) Working memory and vigilance: evidence from normal aging and Alzheimer’s disease. Brain Cogn 41:87–108

    Article  PubMed  CAS  Google Scholar 

  • Blomhoff R, Blomhoff HK (2006) Overview of retinoid metabolism and function. J Neurobiol 66:606–630

    Article  PubMed  CAS  Google Scholar 

  • Blumenfeld RS, Ranganath C (2006) Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. J Neurosci 26:916–925

    Article  PubMed  CAS  Google Scholar 

  • Bohbot VD, Lerch J, Thorndycraft B, Iaria G, Zijdenbos AP (2007) Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J Neurosci 27:10078–10083

    Article  PubMed  CAS  Google Scholar 

  • Bonnet E et al (2008) Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS One 3: e3487

    Google Scholar 

  • Brassen S, Weber-Fahr W, Sommer T, Lehmbeck JT, Braus DF (2006) Hippocampal-prefrontal encoding activation predicts whether words can be successfully recalled or only recognized. Behav Brain Res 171:271–278

    Article  PubMed  Google Scholar 

  • Brouillette J, Quirion R (2008a) Transthyretin: a key gene involved in the maintenance of memory capacities during aging. Neurobiol Aging 29:1721–1732

    Article  PubMed  CAS  Google Scholar 

  • Brouillette J, Quirion R (2008b) The common environmental pollutant dioxin-induced memory deficits by altering estrogen pathways and a major route of retinol transport involving transthyretin. Neurotoxicology 29:318–327

    Article  PubMed  CAS  Google Scholar 

  • Burke SN, Barnes CA (2010) Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 33:153–161

    Google Scholar 

  • Bunge SA, Klingberg T, Jacobsen RB, Gabrieli JDA (2000) A resource model of the neural basis of executive working memory. Proc Natl Acad Sci U S A 97:3573–3578

    Article  PubMed  CAS  Google Scholar 

  • Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30–40

    Article  PubMed  CAS  Google Scholar 

  • Chalfonte BL, Johnson MK (1996) Feature memory and binding in young and older adults. Mem Cognit 24:403–416

    Article  PubMed  CAS  Google Scholar 

  • Chiang MY et al (1998) An essential role for retinoid receptors RARbeta and RXRgamma in long-term potentiation and depression. Neuron 21:1353–1361

    Article  PubMed  CAS  Google Scholar 

  • Cocco S et al (2002) Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 115:475–482

    Article  PubMed  CAS  Google Scholar 

  • Cohen NJ, Poldrack RA, Eichenbaum H (1997) Memory for items and memory for relations in the procedural/declarative memory framework. Memory 5:131–178

    Article  PubMed  CAS  Google Scholar 

  • Cohen NJ et al (1999) Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 9:83–98

    Article  PubMed  CAS  Google Scholar 

  • Corcoran JP, So PL, Maden M (2004) Disruption of the retinoid signalling pathway causes a deposition of amyloid beta in the adult rat brain. Eur J Neurosci 20:896–902

    Article  PubMed  Google Scholar 

  • Craik FI (1990) Changes in memory with normal aging: a functional view. Adv Neurol 51:201–205

    PubMed  CAS  Google Scholar 

  • Crandall J et al (2004) 13-cis-retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice. Proc Natl Acad Sci U S A 101:5111–5116

    Article  PubMed  CAS  Google Scholar 

  • Davachi L, Wagner AD (2002) Hippocampal contributions to episodic encoding: insights from relational and item-based learning. J Neurophysiol 88:982–990

    PubMed  Google Scholar 

  • Ding Y et al (2008) Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer’s disease transgenic mouse model. J Neurosci 28:11622–11634

    Article  PubMed  CAS  Google Scholar 

  • Dunnett SB, Martel FL, Iversen SD (1990) Proactive interference effects on short-term memory in rats: II. Effects in young and aged rats. Behav Neurosci 104:666–670

    Article  PubMed  CAS  Google Scholar 

  • Eichenbaum H, Fagan A, Mathews P, Cohen NJ (1988) Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. Behav Neurosci 102:331–339

    Article  PubMed  CAS  Google Scholar 

  • Eichenbaum H, Mathews P, Cohen NJ (1989) Further studies of hippocampal representation during odor discrimination learning. Behav Neurosci 103:1207–1216

    Article  PubMed  CAS  Google Scholar 

  • Eichenbaum H, Otto T, Cohen NJ (1992) The hippocampus–what does it do? Behav Neural Biol 57:2–36

    Article  PubMed  CAS  Google Scholar 

  • Enderlin V et al (1997) Age-related decreases in mRNA for brain nuclear receptors and target genes are reversed by retinoic acid treatment. Neurosci Lett 229:125–129

    Article  PubMed  CAS  Google Scholar 

  • Etchamendy N et al (2001) Alleviation of a selective age-related relational memory deficit in mice by pharmacologically induced normalization of brain retinoid signaling. J Neurosci 21:6423–6429

    PubMed  CAS  Google Scholar 

  • Etchamendy N, Desmedt A, Cortes-Torrea C, Marighetto A, Jaffard R (2003a) Hippocampal lesions and discrimination performance of mice in the radial maze: sparing or impairment depending on the representational demands of the task. Hippocampus 13:197–211

    Article  PubMed  Google Scholar 

  • Etchamendy N et al (2003b) Vitamin A deficiency and relational memory deficit in adult mice: relationships with changes in brain retinoid signalling. Behav Brain Res 145:37–49

    Article  PubMed  CAS  Google Scholar 

  • Etchamendy N, Konishi K, Pike GB, Marighetto A, Bohbot VD (2011) Evidence for a virtual human analog of a rodent relational memory task: a study of aging and fMRI in young adults. Hippocampus. Jun 8. doi:10.1002/hipo.20948

  • Flicker C, Ferris SH, Crook T, Bartus RT (1989) Age differences in the vulnerability of facial recognition memory to proactive interference. Exp Aging Res 15:189–194

    Article  PubMed  CAS  Google Scholar 

  • Friedman D, Nessler D, Johnson R Jr (2007) Memory encoding and retrieval in the aging brain. Clin EEG Neurosci 38:2–7

    Article  PubMed  Google Scholar 

  • Gabrieli JD (1996) Memory systems analyses of mnemonic disorders in aging and age-related diseases. Proc Natl Acad Sci U S A 93:13534–13540

    Article  PubMed  CAS  Google Scholar 

  • Goodman AB (1998) Three independent lines of evidence suggest retinoids as causal to schizophrenia. Proc Natl Acad Sci U S A 95:7240–7244

    Article  PubMed  CAS  Google Scholar 

  • Goodman AB (2006) Retinoid receptors, transporters, and metabolizers as therapeutic targets in late onset Alzheimer disease. J Cell Physiol 209:598–603

    Article  PubMed  CAS  Google Scholar 

  • Goodman AB, Pardee AB (2003) Evidence for defective retinoid transport and function in late onset Alzheimer’s disease. Proc Natl Acad Sci U S A 100:2901–2905

    Article  PubMed  CAS  Google Scholar 

  • Grady CL (2008) Cognitive neuroscience of aging. Ann NY Acad Sci 1124:127–144

    Article  PubMed  Google Scholar 

  • Grady CL, Craik FI (2000) Changes in memory processing with age. Curr Opin Neurobiol 10:224–231

    Article  PubMed  CAS  Google Scholar 

  • Grady CL, McIntosh AR, Rajah MN, Beig S, Craik FI (1999) The effects of age on the neural correlates of episodic encoding. Cereb Cortex 9:805–814

    Article  PubMed  CAS  Google Scholar 

  • Hannula DE, Ranganath C (2008) Medial temporal lobe activity predicts successful relational memory binding. J Neurosci 28:116–124

    Article  PubMed  CAS  Google Scholar 

  • Hannula DE, Tranel D, Cohen NJ (2006) The long and the short of it: relational memory impairments in amnesia, even at short lags. J Neurosci 26:8352–8359

    Article  PubMed  CAS  Google Scholar 

  • Jinno S (2011) Decline in adult neurogenesis during aging follows a topographic pattern in the mouse hippocampus. J Comp Neurol 519:451–466

    Google Scholar 

  • Jonides J et al (2008) The mind and brain of short-term memory. Annu Rev Psychol 59:193–224

    Article  PubMed  Google Scholar 

  • Kastner P, Mark M, Chambon P (1995) Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83:859–869

    Article  PubMed  CAS  Google Scholar 

  • Krezel W, Kastner P, Chambon P (1999) Differential expression of retinoid receptors in the adult mouse central nervous system. Neuroscience 89:1291–1300

    Article  PubMed  CAS  Google Scholar 

  • Kumaran D (2008) Short-term memory and the human hippocampus. J Neurosci 28:3837–3838

    Article  PubMed  CAS  Google Scholar 

  • Lane MA, Bailey SJ (2005) Role of retinoid signalling in the adult brain. Prog Neurobiol 75:275–293

    Article  PubMed  CAS  Google Scholar 

  • Lee HP et al (2009) All-trans retinoic acid as a novel therapeutic strategy for Alzheimer’s disease. Expert Rev Neurother 9:1615–1621

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre P et al (2005) Transcriptional activities of retinoic acid receptors. Vitam Horm 70:199–264

    Article  PubMed  CAS  Google Scholar 

  • Lund PK et al (2004) Transcriptional mechanisms of hippocampal aging. Exp Gerontol 39:1613–1622

    Article  PubMed  CAS  Google Scholar 

  • Maden M, Sonneveld E, van der Saag PT, Gale E (1998a) The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development 125:4133–4144

    PubMed  CAS  Google Scholar 

  • Maden M, Gale E, Zile M (1998b) The role of vitamin A in the development of the central nervous system. J Nutr 128:471S–475S

    PubMed  CAS  Google Scholar 

  • Malik MA, Blusztajn JK, Greenwood CE (2000) Nutrients as trophic factors in neurons and the central nervous system: role of retinoic acid. J Nutr Biochem 11:2–13

    Article  PubMed  CAS  Google Scholar 

  • Mangelsdorf DJ et al (1995) The nuclear receptor superfamily: the second decade. Cell 83:835–839

    Article  PubMed  CAS  Google Scholar 

  • Marighetto A et al (1999) Knowing which and knowing what: a potential mouse model for age-related human declarative memory decline. Eur J Neurosci 11:3312–3322

    Article  PubMed  CAS  Google Scholar 

  • Marighetto A et al (2000) Further evidence for a dissociation between different forms of mnemonic expressions in a mouse model of age-related cognitive decline: effects of tacrine and S 17092, a novel prolyl endopeptidase inhibitor. Learn Mem 7:159–169

    Article  PubMed  CAS  Google Scholar 

  • Marighetto A et al (2008a) The AMPA modulator S 18986 improves declarative and working memory performances in aged mice. Behav Pharmacol 19:235–244

    Article  PubMed  CAS  Google Scholar 

  • Marighetto A et al (2008b) Comparative effects of the dopaminergic agonists piribedil and bromocriptine in three different memory paradigms in rodents. J Psychopharmacol 22:511–521

    Article  PubMed  CAS  Google Scholar 

  • Marighetto A et al (2008c) Comparative effects of the alpha7 nicotinic partial agonist, S 24795, and the cholinesterase inhibitor, donepezil, against aging-related deficits in declarative and working memory in mice. Psychopharmacology (Berl) 197:499–508

    Article  CAS  Google Scholar 

  • Marill J, Idres N, Capron CC, Nguyen E, Chabot GG (2003) Retinoic acid metabolism and mechanism of action: a review. Curr Drug Metab 4:1–10

    Article  PubMed  CAS  Google Scholar 

  • McCaffery P, Zhang J, Crandall JE (2006) Retinoic acid signaling and function in the adult hippocampus. J Neurobiol 66:780–791

    Article  PubMed  CAS  Google Scholar 

  • Mey J, McCaffery P (2004) Retinoic acid signaling in the nervous system of adult vertebrates. Neuroscientist 10:409–421

    Article  PubMed  CAS  Google Scholar 

  • Mingaud F et al (2007) The hippocampus plays a critical role at encoding discontiguous events for subsequent declarative memory expression in mice. Hippocampus 17:264–270

    Article  PubMed  Google Scholar 

  • Mingaud F et al (2008) Retinoid hyposignaling contributes to aging-related decline in hippocampal function in short-term/working memory organization and long-term declarative memory encoding in mice. J Neurosci 28:279–291

    Article  PubMed  CAS  Google Scholar 

  • Misner DL et al (2001) Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc Natl Acad Sci U S A 98:11714–11719

    Article  PubMed  CAS  Google Scholar 

  • Mitchell KJ, Johnson MK, Raye CL, Mather M, D’Esposito M (2000a) Aging and reflective processes of working memory: binding and test load deficits. Psychol Aging 15:527–541

    Article  PubMed  CAS  Google Scholar 

  • Mitchell KJ, Johnson MK, Raye CL, D’Esposito M (2000b) fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Brain Res Cogn Brain Res 10:197–206

    Article  PubMed  CAS  Google Scholar 

  • Mitchell KJ, Johnson MK, Raye CL, Greene EJ (2004) Prefrontal cortex activity associated with source monitoring in a working memory task. J Cogn Neurosci 16:921–934

    Article  PubMed  Google Scholar 

  • Morcom AM, Good CD, Frackowiak RS, Rugg MD (2003) Age effects on the neural correlates of successful memory encoding. Brain 126:213–229

    Article  PubMed  Google Scholar 

  • Narayanan NS et al (2005) The role of the prefrontal cortex in the maintenance of verbal working memory: an event-related FMRI analysis. Neuropsychology 19:223–232

    Article  PubMed  Google Scholar 

  • Olson IR, Page K, Moore KS, Chatterjee A, Verfaellie M (2006) Working memory for conjunctions relies on the medial temporal lobe. J Neurosci 26:4596–4601

    Article  PubMed  CAS  Google Scholar 

  • Palha JA, Goodman AB (2006) Thyroid hormones and retinoids: a possible link between genes and environment in schizophrenia. Brain Res Rev 51:61–71

    Article  PubMed  CAS  Google Scholar 

  • Poldrack RA, Packard MG (2003) Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41:245–251

    Article  PubMed  Google Scholar 

  • Quinette P et al (2006) The relationship between working memory and episodic memory disorders in transient global amnesia. Neuropsychologia 44:2508–2519

    Article  PubMed  Google Scholar 

  • Rabinowitz JC, Ackerman BP, Craik FI, Hinchley JL (1982) Aging and metamemory: the roles of relatedness and imagery. J Gerontol 37:688–695

    Article  PubMed  CAS  Google Scholar 

  • Ranganath C, Blumenfeld RS (2005) Doubts about double dissociations between short- and long-term memory. Trends Cogn Sci 9:374–380

    Article  PubMed  Google Scholar 

  • Repovs G, Baddeley A (2006) The multi-component model of working memory: explorations in experimental cognitive psychology. Neuroscience 139:5–21

    Article  PubMed  CAS  Google Scholar 

  • Ruano D et al (2008) Association of the gene encoding neurogranin with schizophrenia in males. J Psychiatr Res 42:125–133

    Article  PubMed  Google Scholar 

  • Rypma B, Prabhakaran V, Desmond JE, Gabrieli JD (2001) Age differences in prefrontal cortical activity in working memory. Psychol Aging 16:371–384

    Article  PubMed  CAS  Google Scholar 

  • Sadeh T, Shohamy D, Levy DR, Reggev N, Maril A (2011) Cooperation between the hippocampus and the striatum during episodic encoding. J Cogn Neurosci 23(7):1597–1608 [Epub 28 Jul 2010]

    Article  PubMed  Google Scholar 

  • Sakai Y, Crandall JE, Brodsky J, McCaffery P (2004) 13-cis Retinoic acid (accutane) suppresses hippocampal cell survival in mice. Ann N Y Acad Sci 1021:436–440

    Article  PubMed  CAS  Google Scholar 

  • Salthouse TA, Mitchell DR, Skovronek E, Babcock RL (1989) Effects of adult age and working memory on reasoning and spatial abilities. J Exp Psychol Learn Mem Cogn 15:507–516

    Article  PubMed  CAS  Google Scholar 

  • Saxe MD et al (2007) Paradoxical influence of hippocampal neurogenesis on working memory. Proc Natl Acad Sci U S A 104:4642–4646

    Article  PubMed  CAS  Google Scholar 

  • Schmidtke K, Manner H, Kaufmann R, Schmolck H (2002) Cognitive procedural learning in patients with fronto-striatal lesions. Learn Mem 9:419–429

    Article  PubMed  Google Scholar 

  • Shrager Y, Levy DA, Hopkins RO, Squire LR (2008) Working memory and the organization of brain systems. J Neurosci 28:4818–4822

    Article  PubMed  CAS  Google Scholar 

  • Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231

    Article  PubMed  CAS  Google Scholar 

  • Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci U S A 93:13515–13522

    Article  PubMed  CAS  Google Scholar 

  • Takashima A et al (2006) Successful declarative memory formation is associated with ongoing activity during encoding in a distributed neocortical network related to working memory: a magnetoencephalography study. Neuroscience 139:291–297

    Article  PubMed  CAS  Google Scholar 

  • Wietrzych M et al (2005) Working memory deficits in retinoid X receptor gamma-deficient mice. Learn Mem 12:318–326

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Neurocentre Magendie-Inserm U862, 146 Rue Leo Saignat, 33077, Bordeaux-Cedex, France

    Aline Marighetto & Laurent Brayda-Bruno

  2. NutriNeuro Bordeaux University, avenue des facultés, 33406, Talence, France

    Nicole Etchamendy

Authors
  1. Aline Marighetto
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  2. Laurent Brayda-Bruno
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  3. Nicole Etchamendy
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Correspondence to Aline Marighetto .

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Editors and Affiliations

  1. School of Biomedical Sciences, Inst. Neuroscience, University of Nottingham, Nottingham, NG7 2UH, United Kingdom

    Marie-Christine Pardon

  2. Div. Geriatric Psychiatry, University of California, San Diego, Gilman Drive 9500, La Jolla, 92093-0603, California, USA

    Mark W. Bondi

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Marighetto, A., Brayda-Bruno, L., Etchamendy, N. (2011). Studying the Impact of Aging on Memory Systems: Contribution of Two Behavioral Models in the Mouse. In: Pardon, MC., Bondi, M. (eds) Behavioral Neurobiology of Aging. Current Topics in Behavioral Neurosciences, vol 10. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7854_2011_151

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