The ventral hippocampus is necessary for expressing a spatial memory

Brain Structure and Function

Volumn 217, Issue 1, 2012, Pages 93-106

  Loureiro, Michael ^a   Lecourtier, Lucas ^a   Engeln, Michel ^a,b   Lopez, Joëlle ^a,c   Cosquer, Brigitte ^a   Geiger, Karin ^a   Kelche, Christian ^a   Cassel, Jean Christophe ^a   Pereira De Vasconcelos, Anne ^a  

^a Université de Strasbourg Faculté de Psychologie   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^c Psychology Department   (Canada)

Author keywords

Inactivation; Lidocaine; Morris water maze; Rat; Spatial memory; Ventral hippocampus

Indexed keywords

LIDOCAINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; HIPPOCAMPUS; LOCOMOTION; MALE; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL PERFORMANCE; MOTIVATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; SPATIAL MEMORY; VENTRAL HIPPOCAMPUS;

ANALYSIS OF VARIANCE; ANIMALS; HIPPOCAMPUS; LIDOCAINE; MALE; MAZE LEARNING; MEMORY; RATS; RATS, LONG-EVANS; SPACE PERCEPTION;

RATTUS;

EID: 84856298022     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-011-0332-y     Document Type: Article

References (68)

1. Allen TA, Narayanan NS, Kholodar-Smith DB, Zhao Y, Laubach M, Brown TH (2008) Imaging the spread of reversible brain inactivations using fluorescent muscimol. J Neurosci Methods 171:30-38
2. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591 (Pubitemid 20032948)
3. Ambrogi Lorenzini CG, Baldi E, Bucherelli C, Sacchetti B, Tassoni G (1999) Neural topography and chronology of memory consolidation: a review of functional inactivation findings. Neurobiol Learn Mem 71:1-18 (Pubitemid 29393788)
4. Bannerman DM, Rawlins JNP, McHugh SB, Deacon RMJ, Yee BK, Bast T, Zhang WN, Pothuizen HHJ, Feldon J (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28:273-283 (Pubitemid 38844376)
5. Bartesaghi R, Gessi T, Sperti L (1983) Interlamellar transfer of impulses in the hippocampal formation. Exp Neurol 82:550-567 (Pubitemid 14184289)
6. Bast T (2007) Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behaviour. Rev Neurosci 18:253-281
7. Bast T (2011) The hippocampal learning-behavior translation and the functional significance of hippocampal dysfunction in schizophrenia. Curr Opin Neurobiol 21:1-10
8. Bast T, Wilson IA, Witter MP, Morris RGM (2009) From rapid place learning to behavioural performance: a key role for the intermediate hippocampus. Plos Biol 7:730-746
9. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R (1999) Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400:671-675 (Pubitemid 29382571)
10. Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101:14515-14520 (Pubitemid 39346780)
11. Broadbent NJ, Squire LR, Clark RE (2006) Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learn Mem 13:187-191
12. Christensen T, Bisgaard CF, Nielsen HB, Wiborg O (2010) Transcriptome differentiation along the dorso-ventral axis in laser-captured microdissected rat hippocampal granular cell layer. Neuroscience 170:731-741
13. Corcoran KA, Desmond TJ, Frey KA, Maren S (2005) Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J Neurosci 25:8978-8987 (Pubitemid 41384466)
14. Cosquer B, Pereira de Vasconcelos A, Jürg Fröhlich, Cassel JC (2005) Blood-brain barrier and electromagnetic fields: effects of scopolamine methylbromide on working memory after whole-body exposure to 2.45 GHz microwaves in rats. Behav Brain Res 161:229-237 (Pubitemid 40732405)
15. 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 (Pubitemid 36958283)
16. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW (2009) Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci USA 106:11794-11799
17. Edeline JM, Hars B, Hennevin E, Cotillon N (2002) Muscimol diffusion after intracerebral microinjections: reevaluation based on electrophysiological and autoradiographic quantifications. Neurobiol Learn Mem 78:100-124 (Pubitemid 34713253)
18. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19
19. 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 (Pubitemid 36734879)
20. Floresco SB, Seamans JK, Phillips AG (1996) Differential effects of lidocaine infusions into the ventral CA1/subiculum or the nucleus accumbens on the acquisition and retention of spatial information. Behav Brain Res 81:163-171 (Pubitemid 26384975)
21. Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral strata circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880-1890 (Pubitemid 27089832)
22. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulated cortex in remote contextual fear memory. Science 304:881-883 (Pubitemid 38620189)
23. Gloveli T, Dugladze T, Rotstein HG, Traub RD, Monyer H, Heinemann U, Whittington MA, Kopell NJ (2005) Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc Natl Acad Sci USA 102:13295-13300 (Pubitemid 41325017)
24. Gusev PA, Cui C, Alkon DL, Gubin AN (2005) Topography of Arc/arg3.1 mRNA expression in the dorsal and ventral hippocampus induced by recent and remote spatial memory: dissociation of CA3 and CA1 activation. J Neurosci 25:9384-9397 (Pubitemid 41464751)
25. Hetherington PA, Austin KB, Shapiro ML (1994) Ipsilateral associational pathway in the dentate gyrus: an excitatory feedback system that supports N-methyl-d-aspartate-dependent long-term potentiation. Hippocampus 4:422-438 (Pubitemid 24351899)
26. Howland JG, Harrison RA, Hannesson DK, Phillips AG (2008) Ventral hippocampal involvement in temporal order, but not recognition, memory for spatial information. Hippocampus 18:251-257 (Pubitemid 351399628)
27. Jo YS, Lee I (2010) Disconnection of the hippocampal-perirhinal cortical circuits severely disrupts object-place paired associative memory. J Neurosci 30:9850-9858
28. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99:10825-10830
29. 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 (Pubitemid 351956252)
30. Klement D, Pastalkova E, Fenton A (2005) Tetrodotoxin diffusions into the dorsal hippocampus block non-locomotor place cognition. Hippocampus 15:460-471 (Pubitemid 40916293)
31. Klur S, Muller C, Pereira de Vasconcelos A, Ballard T, Lopez J, Galani R, Certa U, Cassel JC (2009) Hippocampal-dependent spatial memory functions might be lateralized in rats: an approach combining gene expression profiling and reversible inactivation. Hippocampus 19:800-816
32. Koenig J, Cosquer B, Cassel JC (2008) Activation of septal 5-HT1A receptors alters spatial memory encoding, interferes with consolidation, but does not affect retrieval in rats subjected to a water-maze task. Hippocampus 18:99-118
33. Lecourtier L, Pereira de Vasconccelos A, Leroux E, Cosquer B, Geiger K, Lithfous S, Cassel JC (2011) Septohippocampal pathways contribute to system consolidation of a spatial memory: sequential implication of GABAergic and cholinergic neurons. Hipppocampus (in press)
34. Lopez J, Pereira de Vasconcelos A, Cassel JC (2008) Environmental cues saliency influences the vividness of a remote spatial memory in rats. Neurobiol Learn Mem 90:285-289
35. Lopez J, Wolff M, Lecourtier L, Cosquer B, Bontempi B, Dalrymple-Alford J, Cassel JC (2009) The intralaminar thalamic nuclei contribute to remote spatial memory. J Neurosci 29:3302-3306
36. Maggio N, Segal M (2007) Unique regulation of long term potentiation in the rat ventral hippocampus. Hippocampus 17:10-25 (Pubitemid 46218670)
37. Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and pavlovian fear conditioning in rats. Behav Brain Res 88:261-274 (Pubitemid 27496322)
38. Martin JH (1991) Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett 127:160-164
39. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305:96-99 (Pubitemid 38869380)
40. McEown K, Treit D (2009) The role of the dorsal and ventral hippocampus in fear and memory of a shock-probe experience. Brain Res 1251:185-194
41. McEown K, Treit D (2010) Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Res 1353:145-151
42. Micheau J, Riedel G, EvL Roloff, Inglis J, Morris RGM (2004) Reversible hippocampal inactivation partially dissociates how and where to search in the water maze. Behav Neurosci 118:1022-1032 (Pubitemid 39346507)
43. Morris RGM, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683 (Pubitemid 12096189)
44. Moser MB, Moser EI (1998a) Functional differentiation in the hippocampus. Hippocampus 8:608-619 (Pubitemid 29010188)
45. Moser MB, Moser EI (1998b) Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci 18:7535-7542 (Pubitemid 28425835)
46. Moser EI, Moser MB, 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 (Pubitemid 23264375)
47. Moser MB, Moser EI, Forrest E, Andresen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA 92:9697-9701
48. Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the Brain's spatial representation system. Ann Rev Neurosci 31:69-89
49. Nadel L, Hardt O (2011) Update on memory systems and processes. Neuropsychopharmacol Rev 36:251-273
50. Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65-72 (Pubitemid 26112655)
51. Parron C, Poucet B, Save E (2001) Re-evaluation of the spatial memory deficits induced by hippocampal short lasting inactivation reveals the need for cortical co-operation. Behav Brain Res 127:71-79 (Pubitemid 33062404)
52. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144 (Pubitemid 44300243)
53. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic Press, San Diego
54. Pereira de Vasconcelos A, Klur S, Muller C, Cosquer B, Lopez J, Certa U, Cassel JC (2006) Reversible inactivation of the dorsal hippocampus by tetrodotoxin or lidocaine: a comparative study on cerebral functional activity and motor coordination in the rat. Neuroscience 141:1649-1663 (Pubitemid 44251166)
55. Pothuizen HH, Zhang WN, Jongen-Rêlo AL, Feldon J, Yee BK (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 (Pubitemid 38241310)
56. Poucet B, Herrmann T, Buhot MC (1991) Effects of short-lasting inactivations of the ventral hippocampus and medial septum on long-term and short-term acquisition of spatial information in rats. Behav Brain Res 44:53-65
57. Riedel G, Micheau J, Lam AGM, Roloff EVL, 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 (Pubitemid 30602604)
58. Riekkinen P Jr, Ikonen S, Aura J, Riekkinen M (1999) Tetrahydroaminoacridine and d-cycloserine fail to alleviate the water maze spatial navigation defect induced by hippocampal inactivation. Eur J Pharmacol 366:13-18 (Pubitemid 29076715)
59. Rogers JL, Hunsaker MR, Kessner RP (2006) Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiol Learn Mem 86:72-81 (Pubitemid 43792462)
60. Sandkuhler J, Maisch B, Zimmermann M (1987) The use of local anaesthetic microinjections to identify central pathways: a quantitative evaluation of the time course and extent of the neuronal block. Exp Brain Res 68:168-178 (Pubitemid 17153690)
61. Simons JS, Spiers HJ (2003) Prefrontal and medial temporal lobe interactions in long term memory. Nature Rev Neurosci 4:637-648 (Pubitemid 37280159)
62. Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW (2006) Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci 26:7555-7564 (Pubitemid 44315175)
63. Wang GW, Cai JX (2006) Disconnection of the hippocampal-prefrontal cortical circuits impairs spatial working memory performance in rats. Behav Brain Res 175:329-336 (Pubitemid 44750237)
64. Wang GW, Cai JX (2008) Reversible disconnection of the hippocampal-prelimbic cortical circuits impairs spatial learning but not passive avoidance learning in rats. Neurobiol Learn Mem 90:365-373
65. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097 (Pubitemid 44300229)
66. Winocur G, Moscovitch M, Bontempi B (2010) Memory formation and long term retention in humans and animals: convergence towards a transformation account of hippocampal-neocortical interactions. Neuropsychologia 48:2339-2356
67. Witter MP, Amaral DG (2004) Hippocampal formation. In: Paxinos G (ed) In the rat nervous system, Elsevier, Amsterdam, pp 635-704
68. Zhuravin IA, Bures J (1991) Extent of the tetrodotoxin induced blockade examined by papillary paralysis elicited by intracerebral injection of the drug. Exp Brain Res 83:687-690