The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression

Cerebral Cortex

Volumn 18, Issue 4, 2008, Pages 968-977

  Kemp, Anne ^a,b   Manahan Vaughan, Denise ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

CA1; Dentate gyrus; Long term depression; Long term potentiation; Novelty acquisition; Spatial learning

Indexed keywords

ARTICLE; ASSOCIATION; BEHAVIOR; DENTATE GYRUS; ENVIRONMENTAL FACTOR; HIPPOCAMPUS; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; PRIORITY JOURNAL;

ANIMALS; DENTATE GYRUS; ENVIRONMENT; EXCITATORY POSTSYNAPTIC POTENTIALS; EXPLORATORY BEHAVIOR; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; SPACE PERCEPTION; SYNAPSES;

EID: 40849097599     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhm136     Document Type: Article

References (44)

1. Abraham WC, Bear MF. 1996. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19:126-130.
2. Acsady L, Kamondi A, Sik A, Freund T, Buzsaki G. 1998. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci. 18:3386-3403.
3. Amaral DG, Witter MP. 1989. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience. 31:571-591.
4. Barnes CA. 2003. Long-term potentiation and the ageing brain. Philos Trans R Soc Lond B Biol Sci. 358:765-772.
5. Bear MF. 1996. A synaptic basis for memory storage in the cerebral cortex. Proc Natl Acad Sci USA. 93:13453-13459.
6. Bienenstock EL, Cooper LN, Munro PW. 1982. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 2:32-48.
7. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. 1995. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci. 15:47-60.
8. Cassaday HJ, Rawlins JN. 1995. Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. Behav Neurosci. 109:594-606.
9. Cassaday HJ, Rawlins JN. 1997. The hippocampus, objects, and their contexts. Behav Neurosci. 111:1228-1244.
10. Davis CD, Jones FL, Derrick BE. 2004. Novel environments enhance the induction and maintenance of long-term potentiation in the dentate gyrus. J Neurosci. 24:6497-6506.
11. Dragoi G, Harris KD, Buzsaki G. 2003. Place representation within hippocampal networks is modified by long-term potentiation. Neuron. 39:843-853.
12. Fortin NJ, Agster KL, Eichenbaum HB. 2002. Critical role of the hippocampus in memory for sequences of events. Nat Neurosci. 5:458-462.
13. Gilbert PE, Kesner RP, Lee I. 2001. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus. 11:626-636.
14. Gothard KM, Hoffman KL, Battaglia FP, McNaughton BL. 2001. Dentate gyrus and ca1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J Neurosci. 21:7284-7292.
15. Guzowski JF, Knierim JJ, Moser EI. 2004. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron. 44:581-584.
16. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature. 436:801-806.
17. Izquierdo I, Barros DM, Mello e Souza T, de Souza MM, Izquierdo LA, Medina JH. 1998. Mechanisms for memory types differ. Nature. 393:635-636.
18. Izquierdo I, Medina JH, Izquierdo LA, Barros DM, de Souza MM, Mello e Souza T. 1998. Short- and long-term memory are differentially regulated by monoaminergic systems in the rat brain. Neurobiol Learn Mem. 69:219-224.
19. Jacobs LF. 2003. The evolution of the cognitive map. Brain Behav Evol. 62:128-139.
20. Jacobs LF, Schenk F. 2003. Unpacking the cognitive map: the parallel map theory of hippocampal function. Psychol Rev. 110:285-315.
21. Kemp A, Manahan-Vaughan D. 2004. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci USA. 101:8192-8197.
22. Kemp A, Manahan-Vaughan D. 2005. The 5-hydroxytryptamine4 receptor exhibits frequency-dependent properties in synaptic plasticity and behavioural metaplasticity in the hippocampal CA1 region in vivo. Cereb Cortex. 15:1037-1043.
23. Kesner RP, Lee I, Gilbert P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci. 15:333-351.
24. Korz V, Frey JU. 2003. Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors. J Neurosci. 23:7281-7287.
25. Lee I, Yoganarasimha D, Rao G, Knierim JJ. 2004. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature. 430:456-459.
26. Lenck-Santini PP, Rivard B, Muller RU, Poucet B. 2005. Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment. Hippocampus. 15:356-369.
27. Li S, Cullen WK, Anwyl R, Rowan MJ. 2003. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci. 6:526-531.
28. Lisman JE, Otmakhova NA. 2001. Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus. 11:551-568.
29. Manahan-Vaughan D, Braunewell KH. 1999. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci USA. 96:8739-8744.
30. Manahan-Vaughan D, Reiser M, Pin JP, Wilsch V, Bockaert J, Reymann KG, Riedel G. 1996. Physiological and pharmacological profile of trans-azetidine-2,4-dicarboxylic acid: metabotropic glutamate receptor agonism and effects on long-term potentiation. Neuroscience. 72:999-1008.
31. Manahan-Vaughan D, Reymann KG. 1997. Group 1 metabotropic glutamate receptors contribute to slow-onset potentiation in the rat CA1 region in vivo. Neuropharmacology. 36:1533-1538.
32. Nakao K, Ikegaya Y, Yamada MK, Nishiyama N, Matsuki N. 2002. Hippocampal long-term depression as an index of spatial working memory. Eur J Neurosci. 16:970-974.
33. Remondes M, Schuman EM. 2002. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature. 416:736-740.
34. Rolls ET, Kesner RP. 2006. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol. 79:1-48.
35. Shapiro ML, Eichenbaum H. 1999. Hippocampus as a memory map: synaptic plasticity and memory encoding by hippocampal neurons. Hippocampus. 9:365-384.
36. Squire LR, Zola SM. 1996. Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA. 93:13515-13522.
37. Straube T, Korz V, Balschun D, Frey JU. 2003. Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol. 552:953-960.
38. Straube T, Korz V, Frey JU. 2003. Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci Lett. 344:5-8.
39. Vianna MR, Alonso M, Viola H, Quevedo J, de PF, Furman M, de Stein ML, Medina JH, Izquierdo I. 2000. Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem. 7:333-340.
40. Vinogradova OS. 2001. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus. 11:578-598.
41. Vouimba RM, Richter-Levin G. 2005. Physiological dissociation in hippocampal subregions in response to amygdala stimulation. Cereb Cortex. 15:1815-1821.
42. Witter MP, Moser EI. 2006. Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci. 29:671-678.
43. Wood ER, Dudchenko PA, Eichenbaum H. 1999. The global record of memory in hippocampal neuronal activity. Nature. 397:613-616.
44. Xu L, Anwyl R, Rowan MJ. 1997. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature. 387:497-500.