Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory

Neurobiology of Learning and Memory

Volumn 93, Issue 3, 2010, Pages 415-421

  Churchwell, John C ^a   Morris, Andrea M ^a   Musso, Nicholas D ^a   Kesner, Raymond P ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Hippocampus; Navigation; Orbitofrontal cortex; Prefrontal cortex; Spatial

Indexed keywords

LIDOCAINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY CONSOLIDATION; NEUROANATOMY; NONHUMAN; ORBITAL CORTEX; PREFRONTAL CORTEX; RAT; RECALL; SPATIAL MEMORY; TASK PERFORMANCE;

ANIMALS; FUNCTIONAL LATERALITY; HIPPOCAMPUS; MALE; MEMORY; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 77950691281     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.12.008     Document Type: Article

References (54)

1. Bast T. Toward an integrative perspective on hippocampal function: From the rapid encoding of experience to adaptive behavior. Reviews in the Neurosciences 2007, 18(3-4):253-281.
2. Bast T., Wilson I.A., Witter M.P., Morris R.G. From rapid place learning to behavioral performance: A key role for the intermediate hippocampus. PLoS Biology 2009, 7(4):e1000089.
3. Baxter M.G., Parker A., Lindner C.C., Izquierdo A.D., Murray E.A. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. Journal of Neuroscience 2000, 20(11):4311-4319.
4. Burton B.G., Hok V., Save E., Poucet B. Lesion of the ventral and intermediate hippocampus abolishes anticipatory activity in the medial prefrontal cortex of the rat. Behavioural Brain Research 2009, 199(2):222-234.
5. Chang Q., Gold P.E. Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behavioural Brain Research 2003, 144(1-2):19-24.
6. Chang Q., Gold P.E. Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. Journal of Neuroscience 2003, 23(7):3001-3005.
7. Ciaramelli E. The role of ventromedial prefrontal cortex in navigation: A case of impaired wayfinding and rehabilitation. Neuropsychologia 2008, 46(7):2099-2105.
8. Compton D.M., Griffith H.R., McDaniel W.F., Foster R.A., Davis B.K. The flexible use of multiple cue relationships in spatial navigation: A comparison of water maze performance following hippocampal, medial septal, prefrontal cortex, or posterior parietal cortex lesions. Neurobiology of Learning and Memory 1997, 68(2):117-132.
9. Corwin J.V., Fussinger M., Meyer R.C., King V.R., Reep R.L. Bilateral destruction of the ventrolateral orbital cortex produces allocentric but not egocentric spatial deficits in rats. Behavioural Brain Research 1994, 61(1):79-86.
10. de Bruin J.P., Swinkels W.A., de Brabander J.M. Response learning of rats in a Morris water maze: Involvement of the medical prefrontal cortex. Behavioural Brain Research 1997, 85(1):47-55.
11. Feierstein C.E., Quirk M.C., Uchida N., Sosulski D.L., Mainen Z.F. Representation of spatial goals in rat orbitofrontal cortex. Neuron 2006, 51(4):495-507.
12. Floresco S.B., Ghods-Sharifi S. Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cerebral Cortex 2007, 17(2):251-260.
13. Floresco S.B., Seamans J.K., Phillips A.G. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. Journal of Neuroscience 1997, 17(5):1880-1890.
14. Gron G., Wunderlich A.P., Spitzer M., Tomczak R., Riepe M.W. Brain activation during human navigation: Gender-different neural networks as substrate of performance. Nature Neuroscience 2000, 3(4):404-408.
15. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37(5):877-888.
16. Hasselmo M.E. A model of prefrontal cortical mechanisms for goal-directed behavior. Journal of Cognitive Neuroscience 2005, 17(7):1115-1129.
17. Hok V., Lenck-Santini P.P., Roux S., Save E., Muller R.U., Poucet B. Goal-related activity in hippocampal place cells. Journal of Neuroscience 2007, 27(3):472-482.
18. Hok V., Save E., Lenck-Santini P.P., Poucet B. Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proceedings of the National Academy of Sciences USA 2005, 102(12):4602-4607.
19. Hyman J.M., Zilli E.A., Paley A.M., Hasselmo M.E. Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 2005, 15(6):739-749.
20. Jay T.M., Burette F., Laroche S. Plasticity of the hippocampal-prefrontal cortex synapses. Journal of Physiology Paris 1996, 90(5-6):361-366.
21. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology 1991, 313(4):574-586.
22. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biology 2005, 3(12):e402.
23. Kentros C.G., Agnihotri N.T., Streater S., Hawkins R.D., Kandel E.R. Increased attention to spatial context increases both place field stability and spatial memory. Neuron 2004, 42(2):283-295.
24. Kolb B., Buhrmann K., McDonald R., Sutherland R.J. Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cerebral Cortex 1994, 4(6):664-680.
25. Kolb B., Sutherland R.J., Whishaw I.Q. A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. Behavioral Neuroscience 1983, 97(1):13-27.
26. Kyd R.J., Bilkey D.K. Prefrontal cortex lesions modify the spatial properties of hippocampal place cells. Cerebral Cortex 2003, 13(5):444-451.
27. Lee I., Kesner R.P. Encoding versus retrieval of spatial memory: Double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 2004, 14(1):66-76.
28. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 2001, 24:167-202.
29. Hippocampal place fields: Relevance to learning and memory 2008, Oxford University Press, Oxford, New York. S.J. Mizumori (Ed.).
30. Mogensen J., Moustgaard A., Khan U., Wortwein G., Nielsen K.S. Egocentric spatial orientation in a water maze by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex. Brain Research Bulletin 2005, 65(1):41-58.
31. Muzzio I.A., Kentros C., Kandel E. What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. The Journal of Physiology 2009, 587(Pt 12):2837-2854.
32. Ohnishi T., Matsuda H., Hirakata M., Ugawa Y. Navigation ability dependent neural activation in the human brain: An fMRI study. Neuroscience Research 2006, 55(4):361-369.
33. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Clarendon Press, Oxford New York.
34. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65(1):65-72.
35. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2005, Elsevier, Amsterdam, Boston. 5th ed.
36. Ragozzino M.E., Kim J., Hassert D., Minniti N., Kiang C. The contribution of the rat prelimbic-infralimbic areas to different forms of task switching. Behavioral Neuroscience 2003, 117(5):1054-1065.
37. Ragozzino M.E., Wilcox C., Raso M., Kesner R.P. Involvement of rodent prefrontal cortex subregions in strategy switching. Behavioral Neuroscience 1999, 113(1):32-41.
38. Ramus S.J., Davis J.B., Donahue R.J., Discenza C.B., Waite A.A. Interactions between the orbitofrontal cortex and the hippocampal memory system during the storage of long-term memory. Annals of the New York Academy of Sciences 2007, 1121:216-231.
39. Rich E.L., Shapiro M.L. Prelimbic/infralimbic inactivation impairs memory for multiple task switches, but not flexible selection of familiar tasks. Journal of Neuroscience 2007, 27(17):4747-4755.
40. Rich E.L., Shapiro M. Rat prefrontal cortical neurons selectively code strategy switches. Journal of Neuroscience 2009, 29(22):7208-7219.
41. Rogers J.L., Kesner R.P. Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiology of Learning and Memory 2003, 80(3):332-342.
42. Rogers J.L., Kesner R.P. Lesions of the dorsal hippocampus or parietal cortex differentially affect spatial information processing. Behavioral Neuroscience 2006, 120(4):852-860.
43. Rolls E.T., Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology 2006, 79(1):1-48.
44. Rowland D.C., Kentros C.G. Potential anatomical basis for attentional modulation of hippocampal neurons. Annals of the New York Academy of Sciences 2008, 1129:213-224.
45. Seamans J.K., Lapish C.C., Durstewitz D. Comparing the prefrontal cortex of rats and primates: Insights from electrophysiology. Neurotoxicity Research 2008, 14(2-3):249-262.
46. Simons J.S., Spiers H.J. Prefrontal and medial temporal lobe interactions in long-term memory. Nature Reviews Neuroscience 2003, 4(8):637-648.
47. Spiers H.J., Maguire E.A. A navigational guidance system in the human brain. Hippocampus 2007, 17(8):618-626.
48. Sutherland R.J., Kolb B., Whishaw I.Q. Spatial mapping: Definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neuroscience Letters 1982, 31(3):271-276.
49. Vafaei A.A., Rashidy-Pour A. Reversible lesion of the rat's orbitofrontal cortex interferes with hippocampus-dependent spatial memory. Behavioural Brain Research 2004, 149(1):61-68.
50. Vago D.R., Bevan A., Kesner R.P. The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval. Hippocampus 2007, 17(10):977-987.
51. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 2006, 142(1):1-20.
52. Wang G.W., Cai J.X. Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behavioural Brain Research 2006, 175(2):329-336.
53. Wang G.W., Cai J.X. Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats. Neurobiology of Learning and Memory 2008, 90(2):365-373.
54. Winocur G., Moscovitch M. Hippocampal and prefrontal cortex contributions to learning and memory: Analysis of lesion and aging effects on maze learning in rats. Behavioral Neuroscience 1990, 104(4):544-551.