Learning-facilitated synaptic plasticity occurs in the intermediate hippocampus in association with spatial learning

Frontiers in Synaptic Neuroscience

Volumn 5, Issue OCT, 2013, Pages

  Kenney, Jana ^a,b   Manahan Vaughan, Denise ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Dorsoventral axis; In vivo; Intermediate hippocampus; Learning; LTD; LTP; Memory; Rats

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONTROLLED STUDY; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; RAT; SHORT TERM DEPRESSION; SPATIAL LEARNING; SYNAPTIC TRANSMISSION;

EID: 84897429564     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2013.00010     Document Type: Article

References (29)

1. André, M. E., and Manahan-Vaughan, D. (2013). Spatial olfactory learning facilitates long-term depression in the hippocampus. Hippocampus doi: 10.1002/hipo.22158. [Epub ahead of print].
2. Bast, T., Wilson, I. A., Witter, M. P., and Morris, R. G. M. (2009). From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol. 7:e1000089. doi: 10.1371/journal.pbio.1000089
3. Burton, B. G., Hok, V., Save, E., and Poucet, B. (2009). Lesion of the ventral and intermediate hippocampus abolishes anticipatory activity in the medial prefrontal cortex of the rat. Behav. Brain Res. 199, 222-234. doi: 10.1016/j.bbr.2008.11.045
4. Dolorfo, C. L., and Amaral, D. G. (1998). Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 398, 25-48. doi: 10.1002/(SICI)1096-9861(19980817)398:1<25::AID-CNE3>3.0.co;2-B
5. Dong, H. W., Swanson, L. W., Chen, L., Fanselow, M. S., and Toga, A. W. (2009). Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. U.S.A. 106, 11794-11799. doi: 10.1073/pnas.0812608106
6. Fanselow, M. S., and Dong, H. W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures. Neuron 65, 7-19. doi: 10.1016/j.neuron.2009.11.031
7. Goh, J., and Manahan-Vaughan, D. (2013). Spatial object recognition enables endogenous LTD that curtails LTP in the mouse hippocampus. Cereb. Cortex 23, 1118-1125. doi: 10.1093/cercor/bhs089
8. Hagena, H., and Manahan-Vaughan, D. (2011). Learning-facilitated synaptic plasticity at CA3 mossy fiber and commissural-associational synapses reveals different roles in information processing. Cereb. Cortex 21, 2442-2449. doi: 10.1093/cercor/bhq271
9. Harley, C. W. (2007). Norepinephrine and the dentate gyrus. Prog. Brain Res. 163, 299-318. doi: 10.1016/S0079-6123(07)63018-0
10. Kemp, A., and Manahan-Vaughan, D. (2004). Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl. Acad. Sci. U.S.A. 101, 8192-8197. doi: 10.1073/pnas.0402650101
11. Kemp, A., and Manahan-Vaughan, D. (2007). Hippocampal long-term depression: master or minion in declarative memory processes. Trends Neurosci. 30, 111-118. doi: 10.1016/j.tins.2007.01.002
12. Kemp, A., and Manahan-Vaughan, D. (2008). The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression. Cereb. Cortex 18, 968-977. doi: 10.1093/cercor/bhm136
13. Kenney, J., and Manahan-Vaughan, D. (2013). NMDA receptor-dependent synaptic plasticity in dorsal and intermediate hippocampus exhibits distinct frequency-dependent profiles. Neuropharmacology 74, 108-118. doi: 10.1016/j.neuropharm.2013.02.017
14. Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H. A., Murison, R., Moser, E. I., and Moser, M. B. (2002). Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. U.S.A. 99, 10825-10830. doi: 10.1073/pnas.152112399
15. Lemon, N., Aydin-Abidin, S., Funke, K., and Manahan-Vaughan, D. (2009). Locus coeruleus activation facilitates memory encoding and induces hippocampal LTD that depend on beta-adrenoreceptor. Cereb. Cortex 19, 2827-2837. doi: 10.1093/cercor/bhp065
16. Maggio, N., and Segal, M. (2007). Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J. Neurosci. 27, 5757-5765. doi: 10.1523/JNEUROSCI.0155-07.2007
17. Manahan-Vaughan, D., and Braunewell, K. H. (1999). Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl. Acad. Sci. U.S.A. 96, 8739-8744. doi: 10.1073/pnas.96.15.8739
18. Mao, J. B., and Robinson, J. K. (1998). Microinjection of GABA-A agonist muscimol into the dorsal but not the ventral hippocampus impairs non-mnemonic measures of delayed non-matching-to-position performance in rats. Brain Res. 784, 139-147. doi: 10.1016/S0006-8993(97)01324-3
19. Moser, E., Moser, M., and Andersen, P. (1993). Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions but is hardly present following ventral lesions. J. Neurosci. 13, 3916-3925.
20. Moser, E. I., Moser, M. B., and Andersen, P. (1994). Potentiation of dentate synapses initiated by exploratory learning in rats: dissociation from brain temperature, motor activity, and arousal. Learn. Mem. 1, 55-73.
21. Moser, M. B., and Moser, E. I. (1998). Functional differentiation in the hippocampus. Hippocampus 8, 608-619. doi: 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7
22. Moser, M. B., Moser, E. I., Forrest, E., Andersen, P., and Morris, R. G. M. (1995). Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U.S.A. 92, 9697-9701. doi: 10.1073/pnas.92.21.9697
23. Nadel, L. (1967). Behavioral Effects of Dorsal and Ventral Hippocampal Lesions in the Rat. Unpublished Ph.D. thesis, Department of Psychology, McGill University, Montreal.
24. Pothuizen, H. H., Zhang, W. N., Jongen-Relo, A. L., Feldon, J., and Yee, B. K. (2004). Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur. J. Neurosci. 19, 705-712. doi: 10.1111/j.0953-816X.2004.03170.x
25. Ruth, R. E., Collier, T. J., and Routtenberg, A. (1982). Topography between the entorhinal cortex and the dentate septotemporal axis in rats: I. Medial and intermediate entorhinal projecting cells. J. Comp. Neurol. 209, 69-78. doi: 10.1002/cne.902090107
26. Ruth, R. E., Collier, T. J., and Routtenberg, A. (1988). Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats: II. Cells projecting from lateral entorhinal subdivisions. J. Comp. Neurol. 270, 506-516. doi: 10.1002/cne.902700404
27. Sara, S. J., and Bouret, S. (2012). Orienting and reorienting: the locus coeruleus mediates cognition through arousal. Neuron 76, 130-141. doi: 10.1016/j.neuron.2012.09.011
28. Seidenbecher, T., Reymann, K. G., and Balschun, D. (1997). A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc. Natl. Acad. Sci. U.S.A. 94, 1494-1499. doi: 10.1073/pnas.94.4.1494
29. Whitlock, J. R., Heynen, A. J., Shuler, M. G., and Bear, M. F. (2006). Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097. doi: 10.1126/science.1128134