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Gene expression during memory formation

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Abstract

For several decades, neuroscientists have provided many clues that point out the involvement ofde novo gene expression during the formation of longlasting forms of memory. However, information regarding the transcriptional response networks involved in memory formation has been scarce and fragmented. With the advent of genome-based technologies, combined with more classical approaches (i.e., pharmacology and biochemistry), it is now feasible to address those relevant questions-which gene products are modulated, andwhen the processes are necessary for the proper storage of memories- with unprecedented resolution and scale. Using one-trial inhibitory (passive) avoidance training of rats, one of the most studied tasks so far, we found two time windows of sensitivity to transcrip-tional and translational inhibitors infused into the hippocampus: around the time of training and 3–6 h after training. Remarkably, these periods perfectly overlap with the involvement of hippocampal cAMP/PKA (protein kinase A) signaling pathways in memory consolidation. Given the complexity of transcriptional responses in the brain, particularly those related to processing of behavioral information, it was clearly necessary to address this issue with a multi-variable, parallel-oriented approach. We used cDNA arrays to screen for candidate inhibitory avoidance learning-related genes and analyze the dynamic pattern of gene expression that emerges during memory consolidation. These include genes involved in intracellular kinase networks, synaptic function, DNA-binding and chro-matin modification, transcriptional activation and repression, translation, membrane receptors, and oncogenes, among others. Our findings suggest that differential and orchestrated hippocampal gene expression is necessary in both early and late periods of long-term memory consolidation. Additionally, this kind of study may lead to the identification and characterization of genes that are relevant for the pathogenesis of complex psychiatric disorders involving learning and memory impairments, and may allow the development of new methods for the diagnosis and treatment of these diseases.

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References

  • Abel T and KM Lattal (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval.Curr. Opin. Neurobiol. 2, 180–187.

    Article  Google Scholar 

  • Ageta H, A Kato, S Hatakeyama, K Nakayama, Y Isojima and H Sugiyama (2001) Regulation of the level of Vesl-1S/Homer-1a proteins by ubiquitin-proteasome proteolytic systems.J. Biol. Chem. 276, 15893–15897.

    Article  PubMed  CAS  Google Scholar 

  • Agranoff BW, RE Davis and JJ Brink (1965) Memory fixation in the goldfish.Proc. Natl. Acad. Sci. USA 54, 788–793.

    Article  PubMed  CAS  Google Scholar 

  • Atkins CM, JC Selcher, JJ Petraitis, JM Trzaskos and JD Sweatt (1998) The MAPK cascade is required for mammalian associative learning.Nat. Neurosci. 1, 602–609.

    Article  PubMed  CAS  Google Scholar 

  • Balschun D, DP Wolfer, P Gass, T Mantamadiotis, H Welzl, G Schutz, JU Frey and HP Lipp (2003) Does cAMP response element-binding protein have a pivotal role in hippocampal synap-tic plasticity and hippocampus-dependent memory?J. Neurosci. 23, 6304–6314.

    PubMed  CAS  Google Scholar 

  • Barco A, JM Alarcon and ER Kandel (2002) Expression of consti-tutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture.Cell 108, 689–703.

    Article  PubMed  CAS  Google Scholar 

  • Barlow C and DJ Lockhart (2002) DNA arrays and neurobiology--what’s new and what’s next?Curr. Opin. Neurobiol. 12, 554–561.

    Article  PubMed  CAS  Google Scholar 

  • Belotserkovskaya R, S Oh, VA Bondarenko, G Orphanides, VM Studitsky and D Reinberg (2003) FACT facilitates transcription-dependent nucleosome alteration.Science 301, 1090–1093.

    Article  PubMed  CAS  Google Scholar 

  • Bernabeu R, L Bevilaqua, P Ardenghi, E Bromberg, P Schmitz, M Bianchin, I Izquierdo and JH Medina (1997) Involvement of hip-pocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats.Proc. Natl. Acad. Sci. USA 94, 7041–7046.

    Article  PubMed  CAS  Google Scholar 

  • Bertaina V and C Destrade (1995) Differential time courses of c-fos mRNA expression in hippocampal subfields following acquisition and recall testing in mice.Brain Res. Cogn. Brain Res. 2, 269–275.

    Article  PubMed  CAS  Google Scholar 

  • Blanquet PR (2000) Casein kinase 2 as a potentially important enzyme in the nervous system.Prog. Neurobiol. 60, 211–246.

    Article  PubMed  CAS  Google Scholar 

  • Bliss TV and GL Collingridge (1993) A synaptic model of memory: long-term potentiation in the hippocampus.Nature 361, 31–39.

    Article  PubMed  CAS  Google Scholar 

  • Bodian D (1965) A suggestive relationship of nerve cell RNA with specific synaptic sites.Proc. Natl. Acad. Sci. USA 51, 418–425.

    Article  Google Scholar 

  • Bourtchuladze R, T Abel, N Berman, R Gordon, K Lapidus and ER Kandel (1998) Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA.Learn. Mem. 5, 365–374.

    Google Scholar 

  • Brakeman PR, AA Lanahan, R O’Brien, K Roche, CA Barnes, RL Huganir and PF Worley (1997) Homer: a protein that selectively binds metabotropic glutamate receptors.Nature 386, 284–288.

    Article  PubMed  CAS  Google Scholar 

  • Cammarota M, LR Bevilaqua, P Ardenghi, G Paratcha, M Levi de Stein, I Izquierdo and JH Medina (2000) Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade.Brain Res. Mol. Brain Res. 78, 120–130.

    PubMed  Google Scholar 

  • Cammarota M, LR Bevilaqua, H Viola, DS Kerr, B Reichmann, V Teixeira, M Bulla, I Izquierdo and JH Medina (2002) Participation of CaMKII in neuronal plasticity and memory formation.Cell. Mol. Neurobiol. 22, 259–267.

    Article  PubMed  CAS  Google Scholar 

  • Cavallaro S, BG Schreurs, W Zhao, V D’Agata and DL Alkon (2001) Gene expression profiles during long-term memory con solidation.Eur. J. Neurosci. 13, 1809–1815.

    Article  PubMed  CAS  Google Scholar 

  • Cavallaro S, V D’Agata, P Manickam, F Dufour and DL Alkon (2002) Memory-specific temporal profiles of gene expression in the hippocampus.Proc. Natl. Acad. Sci. USA 99, 16279–16284.

    Article  PubMed  CAS  Google Scholar 

  • Clayton DF (2000) The genomic action potential.Neurobiol. Learn. Mem. 74, 185–216.

    Article  PubMed  CAS  Google Scholar 

  • Colantuoni C, AE Purcell, CM Bouton and J Pevsner (2000) High throughput analysis of gene expression in the human brain.J. Neurosci. Res. 59, 1–10.

    Article  PubMed  CAS  Google Scholar 

  • D’Agata V and S Cavallaro (2003) Hippocampal gene expression profiles in passive avoidance conditioning.Eur. J. Neurosci. 18, 2835–2841.

    Article  PubMed  Google Scholar 

  • Davis HP and LR Squire (1984) Protein synthesis and memory: a review.Psychol. Bull. 96, 518–559.

    Article  PubMed  CAS  Google Scholar 

  • Davis RE, PJ Bright and BW Agranoff (1965) Effect of ECS and puromycin on memory in fish.J. Comp. Physiol. Psychol. 60, 162–166.

    Article  PubMed  CAS  Google Scholar 

  • Davis S, B Bozon and S Laroche (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning?Behav. Brain Res. 142, 17–30.

    Article  PubMed  CAS  Google Scholar 

  • Dineley KT, EJ Weeber, C Atkins, JP Adams, AE Anderson and JD Sweatt (2001) Leitmotifs in the biochemistry of LTP induction: amplification, integration and coordination.J. Neurochem. 77, 961–971.

    Article  PubMed  CAS  Google Scholar 

  • Donahue CP, RV Jensen, T Ochiishi, I Eisenstein, M Zhao, T Shors and KS Kosik (2002) Transcriptional profiling reveals regulated genes in the hippocampus during memory formation.Hippocampus 12, 821–833.

    Article  PubMed  CAS  Google Scholar 

  • Dredge BK, AD Polydorides and RB Darnell (2001) The splice of life: alternative splicing and neurological disease.Nat. Rev. Neurosci. 2, 43–50.

    Article  PubMed  CAS  Google Scholar 

  • Dubnau J, AS Chiang, L Grady, J Barditch, S Gossweiler, J McNeil, P Smith, F Buldoc, R Scott, U Certa, C Broger and T Tully (2003) The staufen/pumilio pathway is involved in Drosophila long-term memory.Curr. Biol. 13, 286–296.

    Article  PubMed  CAS  Google Scholar 

  • Eberwine J, B Belt, JE Kacharmina and K Miyashiro (2002) Analysis of subcellularly localized mRNAs usingin situ hybridization, mRNA amplification, and expression profiling.Neurochem. Res. 27, 1065–1077.

    Article  PubMed  CAS  Google Scholar 

  • Flexner LB, JB Flexner and E Stellar (1965) Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin.Exp. Neurol. 13, 264–272.

    Article  PubMed  CAS  Google Scholar 

  • Freeman F, SPR Rose and A Sholey (1995) Two time windows of anisomycin-induced amnesia for passive avoidance training in the day-old chick.Neurobiol. Learn. Mem. 63, 291–295.

    Article  PubMed  CAS  Google Scholar 

  • French PJ, V O’Connor, MW Jones, S Davis, ML Errington, K Voss, B Truchet, C Wotjak, T Stean, V Doyere, M Maroun, S Laroche and TV Bliss (2001) Subfield-specific immediate early gene expression associated with hippocampal long-term potentiationin vivo.Eur. J. Neurosci. 13, 968–976.

    Article  PubMed  CAS  Google Scholar 

  • Garcia RA, K Vasudevan and A Buonanno (2000) The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neu-ronal synapses.Proc. Natl. Acad. Sci. USA 97, 3596–3601.

    Article  PubMed  CAS  Google Scholar 

  • Gerlai R (2002) Hippocampal LTP and memory in mouse strains: is there evidence for a causal relationship?Hippocampus 12, 657–666.

    Article  PubMed  Google Scholar 

  • Gold PE (1986) The use of avoidance training in studies of modulation of memory storage.Behav. Neural Biol. 46, 87–98.

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Pinilla F, V So and JP Kesslak (2001) Spatial learning induces neurotrophin receptor and synapsin I in the hippocampus.Brain Res. 904, 13–19.

    Article  PubMed  CAS  Google Scholar 

  • Grecksch G and M Matthies (1980) Two sensitive periods for the amnestic effect of anisomycin.Pharmacol. Biochem. Behav. 1, 663–665.

    Article  Google Scholar 

  • Guzowski JF, B Setlow, EK Wagner and JL McGaugh (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268.J. Neurosci. 21, 5089–5098.

    PubMed  CAS  Google Scholar 

  • Guzowski JF (2002) Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonu-cleotide and fluorescent imaging approaches.Hippocampus 12, 86–104.

    Article  PubMed  CAS  Google Scholar 

  • Hall J, KL Thomas and BJ Everitt (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning.Nat. Neurosci. 3, 533–535.

    Article  PubMed  CAS  Google Scholar 

  • Henry GL, K Zito and J Dubnau (2003) Chipping away at brain function: mining for insights with microarrays.Curr. Opin. Neurobiol. 13, 570–576.

    Article  PubMed  CAS  Google Scholar 

  • Hevroni D, A Rattner, M Bundman, D Lederfein, A Gabarah, M Mangelus, MA Silverman, H Kedar, C Naor, M Kornuc, T Hanoch, R Seger, LE Theill, E Nedivi, G Richter-Levin and Y Citri (1998) Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms.J. Mol. Neurosci. 10, 75–98.

    Article  PubMed  CAS  Google Scholar 

  • Hirono M, T Sugiyama, Y Kishimoto, I Sakai, T Miyazawa, M Kishio, H Inoue, K Nakao, M Ikeda, S Kawahara, Y Kirino, M Katsuki, H Horie, Y Ishikawa and T Yoshioka (2001) Phospholipase Cbeta4 and protein kinase C? and/or protein kinase CbetaI are involved in the induction of long term depression in cerebellar Purkinje cells.J. Biol. Chem. 276, 45236–45242.

    Article  PubMed  CAS  Google Scholar 

  • Igaz LM, MR Vianna, JH Medina and I Izquierdo (2002) Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning.J. Neurosci. 22, 6781–6789.

    PubMed  CAS  Google Scholar 

  • Igaz LM, P Bekinschtein, I Izquierdo and JH Medina (2004) Changes in hippocampal gene expression during long-term memory consolidation of one-trial inhibitory avoidance learning. Submitted.

  • Izquierdo I and JH Medina (1995) Correlation between the pharmacology of long-term potentiation and the pharmacology of memory.Neurobiol. Learn. Mem. 63, 19–32.

    Article  PubMed  CAS  Google Scholar 

  • Izquierdo I and JH Medina (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures.Neurobiol. Learn. Mem. 68, 285–316.

    Article  PubMed  CAS  Google Scholar 

  • Izquierdo I, C Da Cunha, R Rosat, D Jerusalinsky, JA Quillfeldt, MBC Ferreira and JH Medina (1992) Neurotransmitter receptors involved in memory processing by the amygdala, medial septum and hippocampus of rats.Behav. Neural Biol. 58, 16–25.

    Article  PubMed  CAS  Google Scholar 

  • Izquierdo I, MR Vianna, LA Izquierdo, DM Barros, G Szapiro, AS Coitinho, L Muller, M Cammarota, LR Bevilaqua and JH Medina (2002) Memory retrieval and its lasting consequences.Neurotox. Res. 4, 573–593.

    Article  PubMed  CAS  Google Scholar 

  • Jiang C and EM Schuman (2002) Regulation and function of local protein synthesis in neuronal dendrites.Trends Biochem. Sci. 27, 506–513.

    Article  PubMed  CAS  Google Scholar 

  • Kaczmarek L (2000) Gene expression in learning processes.Acta Neurobiol. Exp. 60, 419–424.

    CAS  Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses.Science 294, 1030–1038.

    Article  PubMed  CAS  Google Scholar 

  • Kato A, Y Fukazawa, F Ozawa, K Inokuchi and H Sugiyama (2003) Activation of ERK cascade promotes accumulation of Vesl-1S/Homer-1a immunoreactivity at synapses.Brain Res. Mol. Brain Res. 118, 33–44.

    Article  PubMed  CAS  Google Scholar 

  • Kelly MP and SA Deadwyler (2003) Experience-dependent regulation of the immediate-early gene arc differs across brain regions.J. Neurosci. 23, 6443–6451.

    PubMed  CAS  Google Scholar 

  • Krichevsky AM and KS Kosik (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation.Neuron 32, 683–696.

    Article  PubMed  CAS  Google Scholar 

  • Lee EH, YP Hsieh, CL Yang, KJ Tsai and CH Liu (2000) Induction of integrin-associated protein (IAP) mRNA expression during memory consolidation in rat hippocampus.Eur. J. Neurosci. 12, 1105–1112.

    Article  PubMed  CAS  Google Scholar 

  • Leil TA, A Ossadtchi, TE Nichols, RM Leahy and DJ Smith (2003) Genes regulated by learning in the hippocampus.J. Neurosci. Res. 71, 763–768.

    Article  PubMed  CAS  Google Scholar 

  • Lin CH, SH Yeh, HY Lu and PW Gean (2003) The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory.J. Neurosci. 23, 8310–8317.

    PubMed  CAS  Google Scholar 

  • Lisman J, H Schulman and H Cline (2002) The molecular basis of CaMKII function in synaptic and behavioural memory.Nat. Rev. Neurosci. 3, 175–190.

    Article  PubMed  CAS  Google Scholar 

  • Lonze BE and DD Ginty (2002) Function and regulation of CREB family transcription factors in the nervous system.Neuron 35, 605–623.

    Article  PubMed  CAS  Google Scholar 

  • Luo Y, JM Long, EL Spangler, DL Longo, DK Ingram and NP Weng (2001) Identification of maze learning-associated genes in rat hippocampus by cDNA microarray.J. Mol. Neurosci. 17, 397–404.

    Article  PubMed  CAS  Google Scholar 

  • Luo Y, JM Long, C Lu, SL Chan, EL Spangler, P Mascarucci, A Raz, DL Longo, MP Mattson, DK Ingram and NP Weng (2002) A link between maze learning and hippocampal expression of neuroleukin and its receptor gp78.J. Neurochem. 80, 354–361.

    Article  PubMed  CAS  Google Scholar 

  • Luo Z and DH Geschwind (2001) Microarray applications in neu-roscience.Neurobiol. Dis. 8, 183–193.

    Article  PubMed  CAS  Google Scholar 

  • Martin SJ and RG Morris (2002) New life in an old idea: the synap-tic plasticity and memory hypothesis revisited.Hippocampus 12, 609–636.

    Article  PubMed  CAS  Google Scholar 

  • Masugi M, M Yokoi, R Shigemoto, K Muguruma, Y Watanabe, G Sansig, H van der Putten and S Nakanishi (1999) Metabotropic glutamate receptor subtype 7 ablation causes deficit in fear response and conditioned taste aversion.J. Neurosci. 19, 955–963.

    PubMed  CAS  Google Scholar 

  • Matsuda S, J Rouault, J Magaud and C Berthet (2001) In search of a function for the TIS21/PC3/BTG1/TOB family.FEBS Lett. 497, 67–72.

    Article  PubMed  CAS  Google Scholar 

  • McGaugh JL (2000) Memory — a century of consolidation.Science 287, 248–251.

    Article  PubMed  CAS  Google Scholar 

  • Meberg PJ, CA Barnes, BL McNaughton and A Routtenberg (1993) Protein kinase C and F1/GAP-43 gene expression in hippocampus inversely related to synaptic enhancement lasting 3 days.Proc. Natl. Acad. Sci. USA 90, 12050–12054.

    Article  PubMed  CAS  Google Scholar 

  • Meberg PJ, WR Kinney, EG Valcourt and A Routtenberg (1996) Gene expression of the transcription factor NF-kappa B in hippocampus: regulation by synaptic activity.Brain Res. Mol. Brain Res. 38, 179–190.

    Article  PubMed  CAS  Google Scholar 

  • Meffert MK, JM Chang, BJ Wiltgen, M Fanselow and D Baltimore (2003) NF-kappaB functions in synaptic signaling and behavior.Nat. Neurosci. 6, 1072–1078.

    Article  PubMed  CAS  Google Scholar 

  • Meister G, C Eggert and U Fischer (2002) SMN-mediated assembly of RNPs: a complex story.Trends Cell Biol. 12, 472–478.

    Article  PubMed  CAS  Google Scholar 

  • Minichiello L, M Korte, D Wolfer, R Kuhn, K Unsicker, V Cestari, C Rossi-Arnaud, HP Lipp, T Bonhoeffer and R Klein (1999) Essential role for TrkB receptors in hippocampus-mediated learning.Neuron 24, 401–414.

    Article  PubMed  CAS  Google Scholar 

  • Mons N, JL Guillou, L Decorte and R Jaffard (2003) Spatial learning induces differential changes in calcium/calmodulin-stimulat-ed (ACI) and calcium-insensitive (ACII) adenylyl cyclases in the mouse hippocampus.Neurobiol. Learn. Mem. 79, 226–235.

    Article  PubMed  CAS  Google Scholar 

  • Montag-Sallaz M and D Montag (2003) Learning-induced arg 3.1/arc mRNA expression in the mouse brain.Learn. Mem. 10, 99–107.

    Article  PubMed  Google Scholar 

  • Neale JH, PD Klinger and BW Agranoff (1973) Camptothecin blocks memory of conditioned avoidance in the goldfish.Science 179, 1243–1246.

    Article  PubMed  CAS  Google Scholar 

  • Nisenbaum LK (2002) The ultimate chip shot: can microarray technology deliver for neuroscience?Genes Brain Behav. 1, 27–34.

    Article  PubMed  CAS  Google Scholar 

  • Paul S, AC Nairn, P Wang and PJ Lombroso (2003) NMDA-medi-ated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling.Nat. Neurosci. 6, 34–42.

    Article  PubMed  CAS  Google Scholar 

  • Pestova TV, VG Kolupaeva, IB Lomakin, EV Pilipenko, IN Shatsky, VI Agol and CU Hellen (2001) Molecular mechanisms of translation initiation in eukaryotes.Proc. Natl. Acad. Sci. USA 98, 7029–7036.

    Article  PubMed  CAS  Google Scholar 

  • Petrovich GD, P Scicli, RF Thompson and LW Swanson (2000) Associative fear conditioning of enkephalin mRNA levels in central amygdalar neurons.Behav. Neurosci. 114, 681–686.

    Article  PubMed  CAS  Google Scholar 

  • Pizarro JM, LS Haro and EJ Barea-Rodriguez (2003) Learning associated increase in heat shock cognate 70 mRNA and protein expression.Neurobiol. Learn. Mem. 79, 142–151.

    Article  PubMed  CAS  Google Scholar 

  • Quevedo J, MRM Vianna, R Roesler, F de Paris, I Izquierdo and SPR Rose (1999) Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: protection from amnesia by pretraining but not pre-exposure to the task apparatus.Learn. Mem. 6, 600–607.

    Article  PubMed  CAS  Google Scholar 

  • Ressler KJ, G Paschall, XL Zhou and M Davis (2002) Regulation of synaptic plasticity genes during consolidation of fear conditioning.J. Neurosci. 22, 7892–7902.

    PubMed  CAS  Google Scholar 

  • Richter-Levin G, KL Thomas, SP Hunt and TV Bliss (1998) Dissociation between genes activated in long-term potentiation and in spatial learning in the rat.Neurosci. Lett. 251, 41–44.

    Article  PubMed  CAS  Google Scholar 

  • Robles Y, PE Vivas-Mejia, HG Ortiz-Zuazaga, J Felix, X Ramos and S Pena de Ortiz (2003) Hippocampal gene expression profiling in spatial discrimination learning.Neurobiol. Learn. Mem. 80, 80–95.

    Article  PubMed  CAS  Google Scholar 

  • Routtenberg A (2001) It’s about time, In Gold PE and WT Greenough (Eds.),Memory Consolidation (American Psychological Association, Washington DC, USA), pp 17–34.

    Google Scholar 

  • Sala C, K Futai, K Yamamoto, PF Worley, Y Hayashi and M Sheng (2003) Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a.J. Neurosci. 23, 6327–6337.

    PubMed  CAS  Google Scholar 

  • Selcher JC, T Nekrasova, R Paylor, GE Landreth and JD Sweatt (2001) Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning.Learn. Mem. 8, 11–19.

    Article  PubMed  CAS  Google Scholar 

  • Shors TJ, G Miesegaes, A Beylin, M Zhao, T Rydel and E Gould (2001) Neurogenesis in the adult is involved in the formation of trace memories.Nature 410, 372–376.

    Article  PubMed  CAS  Google Scholar 

  • Silva AJ, JH Kogan, PW Frankland and S Kida (1998) CREB and memory.Annu. Rev. Neurosci. 21, 127–148.

    Article  PubMed  CAS  Google Scholar 

  • Smith DR, CD Striplin, AM Geller, RB Mailman, J Drago, CP Lawler and M Gallagher (1998) Behavioural assessment of mice lacking D1A dopamine receptors.Neuroscience 86, 135–146.

    Article  PubMed  CAS  Google Scholar 

  • Spencer JA, MH Baron and EN Olson (1999) Cooperative tran-scriptional activation by serum response factor and the high mobility group protein SSRP1.J. Biol. Chem. 274, 15686–15693.

    Article  PubMed  CAS  Google Scholar 

  • Steward O (1997) mRNA localization in neurons: a multipurpose mechanism.Neuron 18, 9–12.

    Article  PubMed  CAS  Google Scholar 

  • Steward O and WB Levy (1982) Preferential localization of polyri-bosomes under the base of dendritic spines in granule cells of the dentate gyrus.J. Neurosci. 2, 284–291.

    PubMed  CAS  Google Scholar 

  • Steward O and EM Schuman (2001) Protein synthesis at synaptic sites on dendrites.Annu. Rev. Neurosci. 24, 299–325.

    Article  PubMed  CAS  Google Scholar 

  • Steward O and PF Worley (2001) Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation.Neuron 30, 227–240.

    Article  PubMed  CAS  Google Scholar 

  • Steward O and P Worley (2002) Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation?Neurobiol. Learn. Mem. 78, 508–527.

    Article  PubMed  CAS  Google Scholar 

  • Tewari M, P Dobrzanski, KL Mohn, DE Cressman, JC Hsu, R Bravo and R Taub (1992) Rapid induction in regenerating liver of RL/IF-1 (an I kappa B that inhibits NF-kappa B, RelB-p50, and c-Rel-p50) and PHF, a novel kappa B site-binding complex.Mol. Cell. Biol. 12, 2898–2908.

    PubMed  CAS  Google Scholar 

  • Thomas U (2002) Modulation of synaptic signalling complexes by Homer proteins.J. Neurochem. 81, 407–413.

    Article  PubMed  CAS  Google Scholar 

  • Tyler WJ, M Alonso, CR Bramham and LD Pozzo-Miller (2002) From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning.Learn. Mem. 9, 224–237.

    Article  PubMed  Google Scholar 

  • Vazdarjanova A, BL McNaughton, CA Barnes, PF Worley and JF Guzowski (2002) Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hip-pocampal and neocortical neuronal networks.J. Neurosci. 22, 10067–10071.

    PubMed  CAS  Google Scholar 

  • Vianna MRM, LA Izquierdo, DM Barros, JH Medina and I Izquierdo (1999) Intrahippocampal infusion of inhibitor of protein kinase A separates short- from long-term memory.Behav. Pharmacol. 10, 223–227.

    PubMed  CAS  Google Scholar 

  • Vianna, MRM, LA Izquierdo, DM Barros, P Ardenghi, P Pereira, C Rodrigues, B Moletta, JH Medina and I Izquierdo (2000) Differential role of hippocampal cAMP-dependent protein kinase in short- and long-term memory.Neurochem. Res. 25, 621–626.

    Article  PubMed  CAS  Google Scholar 

  • Vianna MRM, G Szapiro, JL McGaugh, JH Medina and I Izquierdo (2001) Memory retrieval of a fear-motivated task initiates extinction requiring proteon synthesis in rat hippocampus.Proc. Natl. Acad. Sci. USA 98, 12251–12254.

    Article  PubMed  CAS  Google Scholar 

  • Walz R, R Roesler, DM Barros, MM de Souza, C Rodrigues, MK Sant’Anna, J Quevedo, HK Choi, WP Neto, TL DeDavid e Silva, JH Medina and I Izquierdo (1999) Effects of post-training infusions of a mitogen-activated protein kinase kinase inhibitor into the hippocampus or entorhinal cortex on short- and long-term retention of inhibitory avoidance.Behav. Pharmacol. 10, 723–730.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe Y, K Shiozuka, T Ikeda, N Hoshi, H Hiraki, T Suzuki, S Hashimoto and H Kawashima (1998) Cloning of PCPTP1-Ce encoding protein tyrosine phosphatase from the rat cerebellum and its restricted expression in Purkinje cells.Mol. Brain Res. 58, 83–94.

    Article  PubMed  CAS  Google Scholar 

  • West AE, EC Griffith and ME Greenberg (2002) Regulation of transcription factors by neuronal activity.Nat. Rev. Neurosci. 3, 921–931.

    Article  PubMed  CAS  Google Scholar 

  • Winograd M and H Viola (2004) Detection of novelty, but not memory of spatial habituation, is associated with an increase in phosphorylated cAMP response element-binding protein levels in the hippocampus.Hippocampus 14, 117–123.

    Article  PubMed  CAS  Google Scholar 

  • Xiao B, JC Tu, RS Petralia, JP Yuan, A Doan, CD Breder, A Ruggiero, AA Lanahan, RJ Wenthold and PF Worley (1998) Homer regulates the association of group 1 metabotropic gluta-mate receptors with multivalent complexes of homer-related, synaptic proteins.Neuron 21, 707–716.

    Article  PubMed  CAS  Google Scholar 

  • Xiao B, JC Tu and PF Worley (2000) Homer: a link between neural activity and glutamate receptor function.Curr. Opin. Neurobiol. 10, 370–374.

    Article  PubMed  CAS  Google Scholar 

  • Yin JC and T Tully (1996) CREB and the formation of long-term memory.Curr. Opin. Neurobiol. 2, 264–268.

    Article  Google Scholar 

  • Zhao W, N Meiri, H Xu, S Cavallaro, A Quattrone, L Zhang and DL Alkon (2000) Spatial learning induced changes in expression of the ryanodine type II receptor in the rat hippocampus.FASEB J. 14, 290–300.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Instituto de Biología Celular y Neurociencia Eduardo de Robertis, Facultad de Medicina, Universidad de Buenos Aires, 1113, Buenos Aires, Argentina

    Lionel Muller Igaz, Pedro Bekinschtein & Jorge H. Medina

  2. Centro de Memoria, Departamento de Bioquímica, Instituto de Ciencias Básicas da Saúde, Universidade Federal do Rio Grande do Sul, 90035-003, Porto Alegre, RS, Brasil

    Monica M. R. Vianna & Ivan Izquierdo

Authors
  1. Lionel Muller Igaz
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  2. Pedro Bekinschtein
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  3. Monica M. R. Vianna
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  4. Ivan Izquierdo
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  5. Jorge H. Medina
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Corresponding author

Correspondence to Jorge H. Medina.

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Igaz, L.M., Bekinschtein, P., Vianna, M.M.R. et al. Gene expression during memory formation. neurotox res 6, 189–203 (2004). https://doi.org/10.1007/BF03033221

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  • DOI: https://doi.org/10.1007/BF03033221

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