Hostname: page-component-5c6d5d7d68-wpx84 Total loading time: 0 Render date: 2024-08-08T03:44:35.350Z Has data issue: false hasContentIssue false
  • English
  • Français

Memory formation: its molecular and cell biology

Published online by Cambridge University Press:  13 July 2009

Steven P. R. Rose
Get access Rights & Permissions [Opens in a new window]

Abstract

Memories are stored in the brain in the form of changes in synaptic connectivity brought about through a cascade of molecular processes. Transient synaptic changes result in alterations in gene expression and, ultimately, the synthesis of a family of cell adhesion molecules which are responsible for holding the synapse in a new configuration. However, memory remains a dynamic property of the brain system as a whole, rather than ‘residing’ in any particular small region.

Type
Research Article
Information
European Review , Volume 3 , Issue 3 , July 1995 , pp. 243 - 256
Copyright
Copyright © Academia Europaea 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1.Rose, S. P. R. (1992) The Making of Memory, Bantam Press, London.Google Scholar
2.Hebb, D. O. (1949) The Organisation of Behavior, Wiley, New York.Google Scholar
3.Tanzi, E. (1909) A Text-Book of Mental Diseases (English translation), Rebman, pp. 174–176.Google Scholar
4.Singer, W. (1990) Search for coherence: a basic principle of cortical self-organisation, Conc, Neurosci. 1, 1–26.Google Scholar
5.Goelet, P., Castelluci, V. F., Schacher, S. and Kandel, E. R. (1986) The long and short of long-term memory—a molecular framework, Nature 322, 419–423.CrossRefGoogle Scholar
6.Dudai, Y. (1989) The Neurobiology of Memory, Oxford University Press, Oxford.Google Scholar
7.Ng, K. T. and Gibbs, M. E. (1991) Stages in memory formation: a review. In Andrew, R. J., Ed. Neural and Behavioural Plasticity: The Use of the Domestic Chick as a Model, Oxford University Press, pp. 351–369.CrossRefGoogle Scholar
8.McGaugh, J. L. (1964) Time-dependent processes in memory storage, Science 153, 1351–1358.Google Scholar
9.Davis, H. P. and Squire, L. R. (1984) Protein synthesis and memory: a review, Psychol. Bull. 96, 518–559.CrossRefGoogle ScholarPubMed
10.Rose, S. P. R. (1981) What should a biochemistry of learning and memory be about? Neurosci. 6, 811–821.CrossRefGoogle Scholar
11.Horn, G. (1985) Memory, Imprinting and the Brain, Oxford University Press, Oxford.CrossRefGoogle Scholar
12.Horn, G. (1991) In Andrew, R. J., Ed. Neural and Behavioral Plasticity: The Use of the Domestic Chick as a Model, Oxford University Press, Oxford, pp. 219–261.CrossRefGoogle Scholar
13.Andrew, R. J. (Editor) Behavioural and Neural Plasticity: the use of the Domestic Chick as a Model, Oxford University Press, Oxford.CrossRefGoogle Scholar
14.Cherkin, A. (1969) Kinetics of memory consolidation. Role of amnestic treatment parameters, Proc. Nat. Acad. Sci. 63, 1094–1101.CrossRefGoogle Scholar
15.Rogers, L. J. (1986) Lateralisation of learning in chicks, Adv. Study Behav. 16, 147–189.CrossRefGoogle Scholar
16.Daisley, J. and Rose, S. P. R. (1994) The effect of a passive avoidance task on the release of amino acids in vitro from the left IMHV of the day old chick, Biochem. Sci. Trans. 22, 160S.CrossRefGoogle ScholarPubMed
17.Watkins, J. C. and Collingridge, G. L. (Eds) (1989) The NMDA Receptor, IRL Press, Oxford.Google Scholar
18.Stewart, M. G., Bourne, R. C. and Steele, R. J. (1992) Quantitative autoradiographic demonstration of changes in binding in NMDA-sensitive 3H glutamate and 3H-MK801, but not 3H-AMPA receptors in chick forebrain 30 minutes after passive avoidance training, Eur. J. Neurosci. 4, 936–943.CrossRefGoogle Scholar
19.Morris, R. G. M., Andersen, E., Lynch, G. S. and Baudry, M. (1986) Selective impairment of learning and blockade of long-term potentiation by an NMDA receptor antagonist. Nature 319, 774–776.CrossRefGoogle Scholar
20.Bradley, P., Davies, D. C. and Horn, G. (1985) Connections of the hyperstriatum ventrale of the domestic chick, J. Anat. 140, 577–589.Google ScholarPubMed
21.Garthwaite, J. (1991) Glutamate, nitric oxide and cell–cell signalling in the nervous system, Trends Neurosci. 14, 60–67.CrossRefGoogle ScholarPubMed
22.Bredt, D. S. and Snyder, S. H. (1992) Nitric oxide, a novel neuronal messenger, Neuron 8, 3–11.CrossRefGoogle ScholarPubMed
23.Holscher, C. and Rose, S. P. R. (1994) Inhibitors of phospholipase A2 produce amnesia for a passive avoidance task in the chick, Behav. Neural Biol. 61, 225–232.CrossRefGoogle ScholarPubMed
24.Holscher, C. and Rose, S. P. R. (1992) An inhibitor of nitric oxide synthesis prevents memory formation in the chick, Neurosci. Lett. 145, 189–194.CrossRefGoogle ScholarPubMed
25.Benowitz, L. I. and Routtenberg, A. (1987) A membrane phosphoprotein associated with neuronal development, axonal regeneration, phospholipid metabolism and synaptic plasticity, Trends Neurosci. 10, 527–532.CrossRefGoogle Scholar
26.Bullock, S., De Graan, P. N. E., Oestreicher, A. B., Gispen, W-H. and Rose, S. P. R. (1990) Identification of a 52 kDa chick brain membrane protein showing changed phosphorylation after passive avoidance training as B-50 (GAP 43), Neurosci. Res. Comm. 6, 181–186.Google Scholar
27.Ali, S. M., Bullock, S. and Rose, S. P. R. (1988) Phosphorylation of synaptic proteins in chick forebrain; changes with development and passive avoidance training, J. Neurochem. 50, 1579–1587.CrossRefGoogle ScholarPubMed
28.Akers, R. F., Lovinger, D. M., Colley, D., Linden, D. and Routtenberg, A. (1986) Translocation of protein kinase C activity after LTP may mediate hippocampal synaptic plasticity, Science 231, 587–589.CrossRefGoogle Scholar
29.Linden, D. J. and Routtenberg, A. (1989) The role of protein kinase C in long-term potentiation: a testable model, Brain Res. Rev. 14, 279–296.CrossRefGoogle ScholarPubMed
30.Burchuladze, R., Potter, J. and Rose, S. P. R. (1990) Memory formation in the chick depends on membrane-bound protein kinase C, Brain Res. 535, 131–138.CrossRefGoogle ScholarPubMed
31.Gispen, W-H. and Routtenberg, A. (Eds) (1982; 1986) Phosphoproteins in Neuronal Function. Prog. Brain Res. 58; 69. Elsevier, Amsterdam.Google Scholar
32.Clements, M. P., Rose, S. P. R. and Tiunova, A. (1995) Omega-Conotoxin GVIA disrupts memory formation in the day old chick, Neurobiol. Learn. Mem. In Press.Google Scholar
33.Rosenzweig, M. R., Bennett, E. et al. In. Andrew, R. J. (Ed) Behavioural and Neural Plasticity: the Use of the Domestic Chick as a Model, Oxford, University Press.Google Scholar
34.Chiarugi, V. P., Ruggiero, M. and Coradetti, R. (1989) Oncogenes, protein kinase C, neuronal differentiation and memory, Neurochem. Int. 14, 1–9.Google Scholar
35.Dragunow, M., Currie, R. W., Faull, R. L. M., Robertson, H. A. and Jansen, K. (1989) Immediate-early genes, kindling and long-term potentiation, Neurosci. Biobehav. Rev. 13, 301–313.Google Scholar
36.Cole, A. J., Saffen, D. W.Baraban, J. M. and Worley, P. F. (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation, Nature 340, 474–476.CrossRefGoogle ScholarPubMed
37.Anokhin, K. V., Mileusnic, R., Shamakina, I. and Rose, S. P. R. (1991) Effects of early experience on c-fos gene expression in the chick forebrain, Brain Res. 544, 101–107.CrossRefGoogle ScholarPubMed
38.Anokhin, K. V. and Rose, S. P. R. (1991) Learning-induced increase of immediate early gene messenger RNA in the chick forebrain, Eur. J. Neurosci. 3, 162–167.CrossRefGoogle ScholarPubMed
39.Matthies, H. J. (ED) (1986) Learning and Memory: Mechanisms of Information Storage in the Nervous System, Pergamon Press, Oxford.Google Scholar
40.Matthies, H. J. (1989) In search of cellular mechanisms of memory, Prog. Neurobiol. 32, 277–349.CrossRefGoogle ScholarPubMed
41.Mileusnic, R., Rose, S. P. R. and Tillson, P. (1980) Passive avoidance learning results in region-specific changes in concentration of and incorporation into colchicine-binding proteins in the chick forebrain, J. Neurochem. 34, 1007–1015.CrossRefGoogle ScholarPubMed
42.Scholey, A. B., Bullock, S. and Rose, S. P. R. (1992) Passive avoidance learning in the young chick results in time- and locus-specific elevations of α-tubulin immunoreactivity, Neurochem. Int. 21, 343–350.CrossRefGoogle Scholar
43.Edelman, G. M. (1989) The Remembered Present, Basic Books, New York.Google Scholar
44.Rose, S. P. R. (1995) Glycoproteins and memory formation, Behav. Brain Res. 66, 73–78.CrossRefGoogle ScholarPubMed
45.Bullock, S., Rose, S. P. R. and Zamani, R. (1992) Characterisation and regional localisation of pre- and post-synaptic glycoproteins of the chick forebrain showing changed fucose incorpration following passive avoidance training, J. Neurochem. 58, 2145–2154.CrossRefGoogle Scholar
46.Rose, S. P. R. and Jork, R. (1987) Long-term memory formation in chicks is blocked by 2-deoxygalactose, a fucose analogue, Behav. Neural Biol. 48, 246–268.Google Scholar
47.Doyle, E., Nolan, P., Bell, R. and Regan, C. M. (1992) Hippocampal NCAM-180 transiently increases sialylation during the acquisition and consolidation of a passive avoidance response in the adult rat, J. Neurosci. Res. 31, 513–523.Google Scholar
48.Scholey, A. B., Rose, S. P. R., Zamani, R., Bock, E. and Schachner, M. (1994) A role for the neural cell adhesion molecule in a late consolidating phase of glycoprotein synthesis six hours following passive avoidance training in the young chick, Neurosci. 55, 499–509.CrossRefGoogle Scholar
49.Mileusnic, R., Rose, S. P. R., Lancashire, C. and Bullock, S. (1995) Characterisation of antibodies specific for chick brain NCAM which cause amnesia for a passive avoidance task, J. Neurochem. In Press.CrossRefGoogle ScholarPubMed
50.Barber, A. J., Gilbert, D. B. and Rose, S. P. R. (1989) Glycoprotein synthesis is necessary for memory of sickness-induced learning in chicks, Eur. J. Neurosci. 1, 673–677.CrossRefGoogle ScholarPubMed
51.Bourne, R. C., Davies, D. C., Stewart, M. G., Csillag, A. and Cooper, M. (1991) Cerebral glycoprotein synthesis and long-term memory formation in the chick (gallus domesticus) following passive avoidance training depends on the nature of the aversive stimulus, Eur. J. Neurosci. 3, 243–248.CrossRefGoogle ScholarPubMed
52.Rusakov, D. A., Davies, H. A., Stewart, M. G. and Schachner, M. (1995) Clustering and colocalisation of immunogold double labelled neural cell adhesion molecule isoforms in chick forebrain, Neurosci. Lett. 183, 105.CrossRefGoogle Scholar
53.Bailey, C. H. and Chen, M. (1991) Morphological alterations at identified sensory neuron synapses during long-term sensitisation in Aplysia. In Squire, L. R. and Lindenlaub, E. (Eds) The Biology of Memory, Schattauer Verlag, Stuttgart, pp. 135–154.Google Scholar
54.Patel, S. N. and Stewart, M. G. (1988) Changes in the number and structure of dendritic spines, 25 hr after passive avoidance training in the domestic chick, Gallus domesticus, Brain Res. 449, 34–46.Google Scholar
55.Patel, S. N., Rose, S. P. R. and Stewart, M. G. (1989) Training-induced spine density changes are specifically related to memory formation processes in the chick Gallus domesticus, Brain Res. 463, 168–173.CrossRefGoogle Scholar
56.Stewart, M. G. (1991) In Andrew, R. J. (Ed) Behavioural and Neural Plasticity: the Use of the Domestic Chick as a Model, Oxford University Press, Oxford.Google Scholar
57.Scheich, H., Wallhausser-Franke, E. and Braun, K. (1992) Does synaptic selection explain auditory imprinting. In Memory: Organisation and Locus of Change, Squire, L. R., Weinberger, N. M., Lynch, G. and McGaugh, J. L. (Eds), Oxford University Press, New York, pp. 114–159.CrossRefGoogle Scholar
58.Changeux, J.-P. and Danchin, A. (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks, Nature 264, 705–712.CrossRefGoogle ScholarPubMed
59.Purves, D. (1988) Body and Brain: a Trophic Theory of Neural Connections, Harvard University Press, Cambridge, MA.Google Scholar
60.Purves, D. (1994) Neural Activity and the Growth of the Brain, Cambridge University Press, Cambridge.Google Scholar
61.Mason, R. J. and Rose, S. P. R. (1987) Lasting changes in spontaneous multi-unit activity in the chick brain following passive avoidance training, Neurosci. 21, 931–944.Google Scholar
62.Gigg, J., Patterson, T. A. and Rose, S. P. R. (1993) Training-induced increases in neuronal activity recorded from the forebrain of the day-old chick are time dependent, Neurosci. 56, 771–776.Google Scholar
63.Gigg, J., Patterson, T. A. and Rose, S. P. R. (1994) Increases in neuronal bursting recorded from the chick lobus parolfactorius after training are both time-dependent and memory-specific, Eur. J. Neurosci. 6, 313–319.CrossRefGoogle ScholarPubMed
64.Mason, R. J. and Rose, S. P. R. (1988) Passive avoidance learning produces focal elevation of bursting activity in the chick brain; amnesia abolishes the increase, Behav. Neural Biol. 49, 280–292.CrossRefGoogle ScholarPubMed
65.Rose, S. P. R. (1991) How chicks make memories: the cellular cascade from c-fos to dendritic remodelling, Trends Neurosci. 14, 390–397.CrossRefGoogle ScholarPubMed
66.Sandi, C., Patterson, T. A. and Rose, S. P. R. (1992) Unilateral hippocampal lesions prevent recall of a passive avoidance task in day-old chicks, Neurosci. Lett. 141, 255–258.CrossRefGoogle ScholarPubMed
67.Vallortigara, G., Zanforlin, M. and Compostella, S. (1990) Perceptual organisation in animal learning: cues or objects? Ethology 85, 89–102.Google Scholar
68.Patterson, T. A. and Rose, S. P. R. (1992) Memory in chicks: multiple cues; distinct brain locations, Behav. Neurosci. 106, 465–470.CrossRefGoogle ScholarPubMed
69.Tulving, E. (1991) Interview, J. Cog. Neurosci. 3, 89–94.Google Scholar