Double dissociation between the contributions of the septal and temporal hippocampus to spatial learning: The role of prior experience

Hippocampus

Volumn 24, Issue 8, 2014, Pages 990-1005

  de Hoz, Livia ^a   Martin, Stephen J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Dorsal; Pretraining; Procedural; Ventral; Water maze

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOUBLE DISSOCIATION; HIPPOCAMPUS; LEARNING; LEARNING AND MEMORY TEST; MALE; MEMORY CONSOLIDATION; NONHUMAN; PREOPERATIVE PERIOD; PRIORITY JOURNAL; RAT; SEPTAL HIPPOCAMPUS; SPATIAL LEARNING; SPATIAL MEMORY; TEMPORAL HIPPOCAMPUS; TRAINING; ANIMAL; ASSOCIATION; ENVIRONMENT; MAZE TEST; MEMORY; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CUES; ENVIRONMENT; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; NEUROPSYCHOLOGICAL TESTS; RATS; REVERSAL LEARNING; SPATIAL LEARNING;

EID: 84904247019     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22285     Document Type: Article

References (72)

1. Amaral DG, Witter MP. 1989. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31:571-591.
2. Bannerman DM, Good MA, Butcher SP, Ramsay M, Morris RGM. 1995. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378:182-186.
3. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J. 2004. Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28:273-283.
4. Barkus C, McHugh SB, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM. 2010. Hippocampal NMDA receptors and anxiety: At the interface between cognition and emotion. Eur J Pharmacol 626:49-56.
5. Bast T. 2007. Toward an integrative perspective on hippocampal function: From the rapid encoding of experience to adaptive behavior. Rev Neurosci 18:253-281.
6. Bast T. 2011. The hippocampal learning-behavior translation and the functional significance of hippocampal dysfunction in schizophrenia. Curr Opin Neurobiol 21:492-501.
7. Bast T, Wilson IA, Witter MP, Morris RGM. 2009. From rapid place learning to behavioral performance: A key role for the intermediate hippocampus. PLoS Biol 7:e1000089.
8. Blaha CD, Yang CR, Floresco SB, Barr AM, Phillips AG. 1997. Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens. Eur J Neurosci 9:902-911.
9. Broadbent NJ, Squire LR, Clark RE. 2004. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101:14515-14520.
10. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser MB. 2008. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200-1212.
11. Burton BG, Hok V, Save E, 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.
12. Canals S, Beyerlein M, Merkle H, Logothetis NK. 2009. Functional MRI evidence for LTP-induced neural network reorganization. Curr Biol 19:398-403.
13. de Bruin JP, Sanchez-Santed F, Heinsbroek RP, Donker A, Postmes P. 1994. A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: Evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 652:323-333.
14. de Hoz L, Knox J, Morris RGM. 2003. Longitudinal axis of the hippocampus: Both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus 13:587-603.
15. de Hoz L, Martin SJ, Morris RGM. 2004. Forgetting, reminding, and remembering: The retrieval of lost spatial memory. PLoS Biol 2:E225.
16. Dougherty KA, Islam T, Johnston D. 2012. Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus. J Physiol 590:5707-5722.
17. Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
18. Ferbinteanu J, Ray C, McDonald RJ. 2003. Both dorsal and ventral hippocampus contribute to spatial learning in Long-Evans rats. Neurosci Lett 345:131-135.
19. Floresco SB, Seamans JK, Phillips AG. 1997. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880-1890.
20. Goto Y, Grace AA. 2008. Dopamine modulation of hippocampal-prefrontal cortical interaction drives memory-guided behavior. Cereb Cortex 18:1407-1414.
21. Grace AA, Floresco SB, Goto Y, Lodge DJ. 2007. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
22. Groenewegen HJ, Vermeulen-Van der Zee E, te Kortschot A, Witter MP. 1987. Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience 23:103-120.
23. Groenewegen HJ, Wright CI, Beijer AV. 1996. The nucleus accumbens: Gateway for limbic structures to reach the motor system? Prog Brain Res 107:485-511.
24. Hok V, Save E, Lenck-Santini PP, Poucet B. 2005. Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc Natl Acad Sci USA 102:4602-4607.
25. Hok V, Lenck-Santini PP, Roux S, Save E, Muller RU, Poucet B. 2007. Goal-related activity in hippocampal place cells. J Neurosci 27:472-482.
26. Hyman JM, Zilli EA, Paley AM, Hasselmo ME. 2005. Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 15:739-749.
27. Inglis J, Martin SJ, Morris RGM. 2013. Upstairs/downstairs revisited: spatial pretraining-induced rescue of normal spatial learning during selective blockade of hippocampal N-methyl-D-aspartate receptors. Eur J Neurosci 37:718-727.
28. Ito R, Robbins TW, Pennartz CM, Everitt BJ. 2008. Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J Neurosci 28:6950-6959.
29. Jarrard LE. 1989. On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. J Neurosci Methods 29:251-259.
30. Jay TM, Witter MP. 1991. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313:574-586.
31. Johnson A, van der Meer MA, Redish AD. 2007. Integrating hippocampus and striatum in decision-making. Curr Opin Neurobiol 17:692-697.
32. Jones MW, Wilson MA. 2005. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3:e402.
33. Jung MW, Wiener SI, McNaughton BL. 1994. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347-7356.
34. Kerr KM, Agster KL, Furtak SC, Burwell RD. 2007. Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas. Hippocampus 17:697-708.
35. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB. 2008. Finite scale of spatial representation in the hippocampus. Science 321:140-143.
36. Lacroix L, White I, Feldon J. 2002. Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory. Behav Brain Res 133:69-81.
37. Lepage M, Habib R, Tulving E. 1998. Hippocampal PET activations of memory encoding and retrieval: The HIPER model. Hippocampus 8:313-322.
38. Loureiro M, Lecourtier L, Engeln M, Lopez J, Cosquer B, Geiger K, Kelche C, Cassel JC, Pereira de Vasconcelos A. 2011. The ventral hippocampus is necessary for expressing a spatial memory. Brain Struct Funct 217:93-106.
39. Martin SJ, de Hoz L, Morris RGM. 2005. Retrograde amnesia: Neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia 43:609-624.
40. Micheau J, Riedel G, Roloff EL, Inglis J, Morris RGM. 2004. Reversible hippocampal inactivation partially dissociates how and where to search in the water maze. Behav Neurosci 118:1022-1032.
41. Mogenson GJ, Yang CR. 1991. The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv Exp Med Biol 295:267-290.
42. Moser E, Moser M-B, 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.
43. Moser M-B, Moser EI, Forrest E, Andersen P, Morris RGM. 1995. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA 92:9697-9701.
44. Moser M-B, Moser EI. 1998a. Functional differentiation in the hippocampus. Hippocampus 8:608-619.
45. Moser M-B, Moser EI. 1998b. Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci 18:7535-7542.
46. Morris RG, Shenk F, Tweedie F, Jarrard LE. 1990. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur J Neurosci 2:1016-1028.
47. Naber PA, Witter MP. 1998. Subicular efferents are organized mostly as parallel projections: A double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284-297.
48. Nadel L. 1968. Dorsal and ventral hippocampal lesions and behavior. Physiol Behav 3:891-900.
49. Nadel L, Hoscheidt S, Ryan LR. 2013. Spatial cognition and the hippocampus: The anterior-posterior axis. J Cog Neurosci 25:22-28.
50. Otnaess MK, Brun VH, Moser M-B, Moser EI. 1999. Pretraining prevents spatial learning impairment after saturation of hippocampal long-term potentiation. J Neurosci 19:RC49.
51. Poppenk J, Evensmoen HR, Moscovitch M, Nadel L. 2013. Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230-240.
52. Riedel G, Micheau J, Lam AG, Roloff EL, Martin SJ, Bridge H, de Hoz L, Poeschel B, McCulloch J, Morris RGM. 1999. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2:898-905.
53. Ruediger S, Spirig D, Donato F, Caroni P. 2012. Goal-oriented searching mediated by ventral hippocampus early in trial-and-error learning. Nat Neurosci 15:1563-1571.
54. Saucier D, Cain DP. 1995. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378:186-189.
55. Seamans JK, Floresco SB, Phillips AG. 1998. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J Neurosci 18:1613-1621.
56. Small SA. 2002. The longitudinal axis of the hippocampal formation: Its anatomy, circuitry, and role in cognitive function. Rev Neurosci 13:183-194.
57. Smith CN, Wixted JT, Squire LR. 2011. The hippocampus supports both recollection and familiarity when memories are strong. J Neurosci 31:15693-15702.
58. Sparks FT, Lehmann H, Sutherland RJ. 2011. Between-systems memory interference during retrieval. Eur J Neurosci 34:780-786.
59. Spooner RI, Thomson A, Hall J, Morris RG, Salter SH. 1994. The Atlantis platform: A new design and further developments of Buresova's on-demand platform for the water maze. Learn Mem 1:203-211.
60. Swanson LW. 1981. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 217:150-154.
61. Taepavarapruk P, Howland JG, Ahn S, Phillips AG. 2008. Neural circuits engaged in ventral hippocampal modulation of dopamine function in medial prefrontal cortex and ventral striatum. Brain Struct Funct 213:183-195.
62. Takashima A, Nieuwenhuis IL, Jensen O, Talamini LM, Rijpkema M, Fernandez G. 2009. Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29:10087-10093.
63. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM. 2007. Schemas and memory consolidation. Science 316:76-82.
64. Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, Bito H, Morris RGM. 2011. Schema-dependent gene activation and memory encoding in neocortex. Science 333:891-895.
65. Tulving E. 1985. How many memory systems are there? Am Psychol 40:385-398.
66. van der Meer MA, Redish AD. 2011a. Theta phase precession in rat ventral striatum links place and reward information. J Neurosci 31:2843-2854.
67. van der Meer MA, Redish AD. 2011b. Ventral striatum: A critical look at models of learning and evaluation. Curr Opin Neurobiol 21:387-392.
68. van Groen T, Wyss JM. 1990. Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp.Neurology 302:515-528.
69. van Kesteren MT, Fernandez G, Norris DG, Hermans EJ. 2010. Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci USA 107:7550-7555.
70. Wang SH, Finnie PS, Hardt O, Nader K. 2012a. Dorsal hippocampus is necessary for novel learning but sufficient for subsequent similar learning. Hippocampus 22:2157-2170.
71. Wang SH, Tse D, Morris RGM. 2012b. Anterior cingulate cortex in schema assimilation and expression. Learn Mem 19:315-318.
72. Yu SS, Johnson JD, Rugg MD. 2012. Hippocampal activity during recognition memory co-varies with the accuracy and confidence of source memory judgments. Hippocampus 22:1429-1437.