Altered plasticity in hippocampal CA1, but not dentate gyrus, following long-term environmental enrichment

Journal of Neurophysiology

Volumn 103, Issue 6, 2010, Pages 3320-3329

  Eckert, Michael J ^a   Bilkey, David K ^a   Abraham, Wickliffe C ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; DENTATE GYRUS; ELECTRIC STIMULATION; ENVIRONMENT; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MAZE LEARNING; MEMORY; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SYNAPTIC TRANSMISSION;

EID: 77953520544     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01037.2009     Document Type: Article

References (42)

1. Abraham WC, Mason-Parker SE, Irvine GI, Logan B, Gill AI. Induction and activity-dependent reversal of persistent LTP and LTD in lateral perforant path synapses in vivo. Neurobiol Learn Mem 86:82-90, 2006.
2. Abraham WC, Logan B, Greenwood JM, Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci 22: 9626-9634, 2002. (Pubitemid 35356205)
3. Artola A, von Frijtag JC, Fermont PC, Gispen WH, Schrama LH, Kamal A, Spruijt BM. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioral stress and environmental enrichment. Eur J Neurosci 23: 261-272, 2006.
4. Duffy SN, Craddock KJ, Abel T, Nguyen PV. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus- dependent memory. Learn Mem 8: 26-34, 2001.
5. Eckert MJ, Bilkey DK, Crandall J, Cheyne K, Lu X, Chowdhury A, Worley P, Abraham WC. Environmental enrichment increases the sparseness of spatial representations in the hippocampus. Soc Neurosci Abstr 641, 2007.
6. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, Sopher B, Martin GM, Kim S, Langdon RB, Sisodia SS, Tsien JZ. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32: 911-926, 2001.
7. Finelli LA, Haney S, Bazhenov M, Stopfer M, Sejnowski TJ. Synaptic learning rules and sparse coding in a model sensory system. PLoS Comput Biol 4: e1000062, 2008.
8. Foster TC, Dumas TC. Mechanism for increased hippocampal synaptic strength following differential experience. J Neurophysiol 85: 1377-1383, 2001.
9. Foster TC, Fugger HN, Cunningham SG. Receptor blockade reveals a correspondence between hippocampal-dependent behavior and experience-dependent synaptic enhancement. Brain Res 87: 39-43, 2000.
10. Foster TC, Gagne J, Massicotte G. Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Res 736: 243-250, 1996.
11. Green EJ, Greenough WT. Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. J Neurophysiol 55: 739-750, 1986.
12. Gresack JE, Risbrough VB, Scott CN, Coste S, Stenzel-Poore M, Geyer MA, Powell SB. Isolation rearing-induced deficits in contextual fear learning do not require CRF(2) receptors. Behav Brain Res 209: 80-84, 2010.
13. Hebb D. The Organization of Behavior: A Neuropsychological Theory. New York: Wiley, 1949.
14. Ibi D, Takuma K, Koike H, Mizoguchi H, Tsuritani K, Kuwahara Y, Kamei H, Nagai T, Yoneda Y, Nabeshima T, Yamada K. Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J Neurochem 105: 921-932, 2008.
15. Irvine GI, Abraham WC. Enriched environment exposure alters the input-output dynamics of synaptic transmission in area CA1 of freely moving rats. Neurosci Lett 391: 32-37, 2005.
16. Irvine GI, Logan B, Eckert M, Abraham WC. Enriched environment exposure regulates excitability, synaptic transmission, and LTP in the dentate gyrus of freely moving rats. Hippocampus 16: 149-160, 2006.
17. Jankowsky JL, Melnikova T, Fadale DJ, Xu GM, Slunt HH, Gonzales V, Younkin LH, Younkin SG, Borchelt DR, Savonenko AV. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci 25: 5217-5224, 2005.
18. Kemp A, Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci USA 101: 8192-8197, 2004.
19. Kempermann G, Gast D, Gage FH. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52: 135-143, 2002.
20. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495, 1997.
21. Kirov SA, Petrak LJ, Fiala JC, Harris KM. Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 127: 69-80, 2004.
22. Kobayashi S, Ohashi Y, Ando S. Effects of enriched environments with different durations and starting times on learning capacity during aging in rats assessed by a refined procedure of the Hebb-Williams maze task. J Neurosci Res 70: 340-346, 2002.
23. Koike H, Ibi D, Mizoguchi H, Nagai T, Nitta A, Takuma K, Nabeshima T, et al. Behavioral abnormality and pharmacologic response in social isolation-reared mice. Behav Brain Res 202: 114-121, 2009.
24. Laviola G, Hannan AJ, Macré S, Solinas M, Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31: 159-168, 2008.
25. Lazarov O, Robinson J, Tang Y, Hairston IS, Korade-Mirnics Z, Lee VM, Hersh LB, Sapolsky RM, Mirnics K, Sisodia SS. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120: 701-713, 2005.
26. Liu P, Bilkey DK. The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav Neurosci 115: 94-111, 2001. (Pubitemid 32185154)
27. Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci USA 96: 8739-8744, 1999.
28. McClelland JL, McNaughton BL, O'Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102: 419-457, 1995.
29. Mockett B, Coussens C, Abraham WC. NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation. Eur J Neurosci 15: 1819-1826, 2002.
30. Nithianantharajah J, Barkus C, Murphy M, Hannan AJ. Gene-environment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington's disease transgenic mice. Neurobiol Dis 29: 490-504, 2008.
31. Ohlsson AL, Johansson BB. Environment influences functional outcome of cerebral infarction in rats. Stroke J Cereb Circ 26: 644-649, 1995.
32. Parsley SL, Pilgram SM, Soto F, Giese KP, Edwards FA. Enriching the environment of alphaCaMKIIT286A mutant mice reveals that LTD occurs in memory processing but must be subsequently reversed by LTP. Learn Mem 14: 75-83, 2007.
33. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC. Storage of spatial information by the maintenance mechanism of LTP. Science 313: 1141-1144, 2006.
34. Pham TM, Ickes B, Albeck D, Söderström S, Granholm AC, Mohammed AH. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94: 279-286, 1999.
35. Rolls ET, Kesner RP. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79: 1-48, 2006.
36. Schrijver NC, Pallier PN, Brown VJ, Würbel H. Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behav Brain Res 152: 307-314, 2004.
37. Teather LA, Magnusson JE, Chow CM, Wurtman RJ. Environmental conditions influence hippocampus-dependent behaviors and brain levels of amyloid precursor protein in rats. Eur J Neurosci 16: 2405-2415, 2002.
38. Turrigiano GG. Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22: 221-227, 1999.
39. Turrigiano. GG. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135: 422-435, 2008.
40. Weiss IC, Pryce CR, Jongen-Rêlo AL, Nanz-Bahr NI, Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Re 152: 279-295, 2004.
41. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097, 2006.
42. Young D, Lawlor PA, Leone P, Dragunow M, During MJ. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 5: 448-453, 1999.