Spatial memory tasks in rodents: What do they model?

Cell and Tissue Research

Volumn 354, Issue 1, 2013, Pages 273-286

  Morellini, Fabio ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Declarative memory; Episodic memory; Procedural memory; Spatial memory; Working memory

Indexed keywords

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; EPISODIC MEMORY; EXPERIMENTAL ANIMAL; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; FUNCTIONAL ANATOMY; FUNCTIONAL DISSOCIATION; LONG TERM MEMORY; MAZE TEST; MEMORY DISORDER; MENTAL PERFORMANCE; MENTAL TASK; NEUROANATOMY; NEUROPSYCHIATRY; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; REFERENCE MEMORY; REVIEW; RODENT; SHORT TERM MEMORY; SPATIAL LEARNING; SPATIAL MEMORY; WORKING MEMORY; ANIMAL; ANIMAL MODEL; COGNITION; HUMAN; MEMORY; MOUSE; PHYSIOLOGY; RAT;

ANIMALIA; MUS; RATTUS; RODENTIA;

ANIMALS; COGNITION; HUMANS; MEMORY; MICE; MODELS, ANIMAL; RATS; RODENTIA;

EID: 84885625192     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1668-9     Document Type: Review

References (126)

1. Adolphs R, Tranel D, Buchanan TW (2005) Amygdala damage impairs emotional memory for gist but not details of complex stimuli. Nat Neurosci 8:512-518 (Pubitemid 41007570)
2. Aggleton JP, Neave N, Nagle S, Sahgal A (1995) A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions. J Neurosci 15:7270-7281
3. Almkvist O, Winblad B (1999) Early diagnosis of Alzheimer dementia based on clinical and biological factors. Eur Arch Psychiatry Clin Neurosci 249(Suppl 3):3-9
4. Anderson JR (1976) Language, memory, and thought. Erlbaum, Hillsdale
5. Atkinson RC, Shiffrin RM (1968) Human memory: a proposed system and its control processes. In: Spence KW, Spence JT (eds) The psychology of learning and motivation, vol 2. Academic Press, Oxford, pp 89-195
6. Baddeley A (1992) Working memory. Science 255:556-559
7. Baddeley AD, Warrington EK (1970) Amnesia and the distinction between long- and short-term memory. J Verbal Learn Verbal Behav 9:176-189
8. 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
9. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113:1170-1178
10. Barch DM, Ceaser A (2012) Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci 6:27-34
11. Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65-94 (Pubitemid 127705285)
12. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269:1115-1118
13. Becker JT, Morris RG (1999) Working memory(s). Brain Cogn 41:1-8 (Pubitemid 29487525)
14. Benus RF, Bohus B, Koolhaas JM, Oortmerssen GA von (1989) Behavioural strategies of aggressive and non-aggressive male mice in active shock avoidance. Behav Process 20:1-12
15. Boyer P, Phillips JL, Rousseau FL, Ilivitsky S (2007) Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res Rev 54:92-112 (Pubitemid 46509660)
16. Brandewiede J, Schachner M, Morellini F (2005) Ethological analysis of the senescence-accelerated P/8 mouse. Behav Brain Res 158:109-121 (Pubitemid 40174716)
17. Burgess N, Maguire EA, O'Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625-641 (Pubitemid 35223024)
18. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130-138
19. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature 377:295-296
20. Cain DP (1998) Testing the NMDA, long-term potentiation, and cholinergic hypotheses of spatial learning. Neurosci Biobehav Rev 22:181-193 (Pubitemid 28194377)
21. Cave C, Squire LR (1992) Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus 2:151-163
22. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, Morris RG (2000) A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408:975-979 (Pubitemid 32101643)
23. Cheng K (1986) A purely geometric module in the rat's spatial representation. Cognition 23:149-178
24. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272-278
25. Clayton NS, Yu KS, Dickinson A (2003) Interacting cache memories: evidence of flexible memory use by scrub jays. J Exp Psychol Anim Behav Process 29:1-22
26. Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory. Nature 386:604-608
27. Cohen NJ, Eichenbaum H (1993) Memory amnesia and the hippocampal system. MIT Press, Cambridge
28. Cole MR, Chappell-Stephenson R (2003) Exploring the limits of spatial memory using very large mazes. Learn Behav 31:349-368 (Pubitemid 38622767)
29. Corkin S (2002) What's new with the amnesic patient H.M.? Nat Rev Neurosci 3:153-160 (Pubitemid 135706584)
30. Deacon RM, Bannerman DM, Kirby BP, Croucher A, Rawlins JN (2002) Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res 133:57-68
31. Deacon RM, Penny C, Rawlins JN (2003) Effects of medial prefrontal cortex cytotoxic lesions in mice. Behav Brain Res 139:139-155 (Pubitemid 36300790)
32. Dere E, Huston JP, De Souza Silva MA (2005) Episodic-like memory in mice: simultaneous assessment of object, place and temporal order memory. Brain Res Protocol 16:10-19 (Pubitemid 41774066)
33. D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 36:60-90 (Pubitemid 32763130)
34. Drachman DA, Arbit J (1966) Memory and the hippocampal complex. II. Is memory a multiple process? Arch Neurol 15:52-61
35. Drago V, Babiloni C, Bartrés-Faz D, Caroli A, Bosch B, Hensch T, Didic M, Klafki HW, Pievani M, Jovicich J, Venturi L, Spitzer P, Vecchio F, Schoenknecht P, Wiltfang J, Redolfi A, Forloni G, Blin O, Irving E, Davis C, Hårdemark HG, Frisoni GB (2011) Disease tracking markers for Alzheimer's disease at the prodromal (MCI) stage. J Alzheimers Dis 26:159-199
36. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86 (Pubitemid 40517787)
37. Dudchenko PA (2004) An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev 28:699-709 (Pubitemid 39535867)
38. Dusek JA, Eichenbaum H (1997) The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci USA 94:7109-7171
39. Eichenbaum H (2001) The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 127:199-207 (Pubitemid 33062410)
40. Eichenbaum H, Dusek J, Young B, Bunsey M (1996) Neural mechanisms of declarative memory. Cold Spring Harb Symp Quant Biol 61:197-206 (Pubitemid 27257968)
41. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H (1999) The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23:209-226 (Pubitemid 29315717)
42. Elgh E, Domellof M, Linder J, Edstrom M, Stenlund H, Forsgren L (2009) Cognitive function in early Parkinson's disease: a population-based study. Eur J Neurol 16:1278-1284
43. 2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22:7177-7194 (Pubitemid 35379172)
44. Eysenck MW (1988) Models of memory: information processing. Psychopharmacol Ser 6:3-11
45. Fellini L, Morellini F (2011) Geometric information is required for allothetic navigation in mice. Behav Brain Res 222:380-384
46. Fellini L, Morellini F (2013) Mice create what-where-when hippocampus-dependent memories of unique experiences. J Neurosci 33:1038-1043
47. Fellini L, Schachner M, Morellini F (2006) Adult but not aged C57BL/6 male mice are capable of using geometry for orientation. Learn Mem 13:473-481 (Pubitemid 44157473)
48. Förstl H, Kurz A (1999) Clinical features of Alzheimer's disease. Eur Arch Psychiatry Clin Neurosci 249:288-290 (Pubitemid 30011730)
49. Fuster JM, Bauer RH, Jervey JP (1982) Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Exp Neurol 77:679-694 (Pubitemid 12011180)
50. Gabrieli J, Kao Y (2007) Development of the declarative memory system in the human brain. Nat Neurosci 10:1198-1205 (Pubitemid 47339950)
51. Gazzaley A, Cooney JW, McEvoy K, Knight RT, D'Esposito M (2005) Top-down enhancement and suppression of the magnitude and speed of neural activity. J Cogn Neurosci 17:507-517 (Pubitemid 40364537)
52. Gerlai R (1998) A new continuous alternation task in a T-maze detects hippocampal dysfunction in mice: a strain comparison and lesion study. Behav Brain Res 95:91-101 (Pubitemid 28400375)
53. Gerlai R (2001) Behavioral tests of hippocampal function: simple paradigms complex problems. Behav Brain Res 125:269-277 (Pubitemid 33000465)
54. Goldman-Rakic PS (1994) Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 6:348-357 (Pubitemid 24344855)
55. Graham KS, Barense MD, Lee ACH (2010) Going beyond LTM in the MTL: a synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia 48:831-853
56. Griffiths D, Whalsten D (1974) Interacting effects of handling and D-amphetamine on avoidance learning. Pharmacol Biochem Behav 2:439-444
57. Griffiths DP, Dickinson A, Clayton NS (1999) Declarative and episodic memory: what can animals remember about their past? Trends Cogn Sci 3:74-80 (Pubitemid 29099881)
58. Hasselmo ME (2012) How we remember: brain mechanisms of episodic memory. MIT Press, Cambridge
59. Hodges H (1996) Maze procedures: the radial-arm and water maze compared. Brain Res Cogn Brain Res 3:167-168
60. Huber SJ, Paulson GW (1985) The concept of subcortical dementia. Am J Psychiatry 142:1312-1317 (Pubitemid 16216568)
61. Hughes RN (2004) The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neurosci Biobehav Rev 28:497-505 (Pubitemid 39311449)
62. Jakovcevski M, Schachner M, Morellini F (2008) Individual variability in the stress response of C57BL/6J male mice correlates with trait anxiety. Genes Brain Behav 7:235-243 (Pubitemid 351342200)
63. Jakovcevski M, Schachner M, Morellini F (2011) Susceptibility to the long-term anxiogenic effects of an acute stressor is mediated by the activation of the glucocorticoid receptors. Neuropharmacology 61:1297-1305
64. Kenworthy L, Yerys BE, Anthony LG, Wallace GL (2008) Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychol Rev 18:320-338
65. Kesner RP, Churchwell JC (2011) An analysis of rat prefrontal cortex in mediating executive function. Neurobiol Learn Mem 96:417-431
66. Knierim JJ, Hamilton DA (2011) Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol Rev 91:1245-1279
67. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399-1402 (Pubitemid 26296530)
68. Law JW, Lee AY, Sun M, Nikonenko AG, Chung SK, Dityatev A, Schachner M, Morellini F (2003) Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci 23:10419-10432 (Pubitemid 37444619)
69. Lenck-Santini PP, Save E, Poucet B (2001) Place-cell firing does not depend on the direction of turn in a Y-maze alternation task. Eur J Neurosci 13:1055-1058 (Pubitemid 32226158)
70. Lipp HP, Wolfer DP (1998) Genetically modified mice and cognition. Curr Opin Neurobiol 8:272-280 (Pubitemid 28247811)
71. Liston C, Malter Cohen M, Teslovich T, Levenson D, Casey BJ (2011) Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point? Biol Psychiatry 69:1168-1177
72. Maei HR, Zaslavsky K, Teixeira CM, Frankland PW (2009) What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 3:4
73. Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR (2003) Recognition memory and the human hippocampus. Neuron 37:171-180 (Pubitemid 36106443)
74. McClelland JL, McNaughton BL, O'Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychiatr Rev 102:419-457
75. McGaugh JL (2000) Memory-a century of consolidation. Science 287:248-251
76. McIntyre JS, Craik FI (1987) Age differences in memory for item and source information. Can J Psychol 41:175-192
77. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173-185 (Pubitemid 126603950)
78. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the cognitive map. Nat Rev Neurosci 7:663-678 (Pubitemid 44106748)
79. Meier I, Fellini L, Jakovcevski M, Schachner M, Morellini F (2010) Expression of the snoRNA host gene gas5 in the hippocampus is upregulated by age and psychogenic stress and correlates with reduced novelty-induced behavior in C57BL/6 mice. Hippocampus 20:1027-1036
80. Miller GA (1956) The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychol Rev 63:81-97
81. Miller DB, O'Callaghan JP (2005) Aging, stress and the hippocampus. Ageing Res Rev 4:123-140 (Pubitemid 41111977)
82. Milner B (1972) Disorders of learning and memory after temporal lobe lesions in man. Clin Neur 19:421-466
83. Morellini F, Schachner M (2006) Enhanced novelty-induced activity, reduced anxiety, delayed resynchronization to daylight reversal and weaker muscle strength in tenascin-C-deficient mice. Eur J Neurosci 23:1255-1268
84. Morellini F, Sivukhina E, Stoenica L, Oulianova E, Bukalo O, Jakovcevski I, Dityatev A, Irintchev A, Schachner M (2010) Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus. Cereb Cortex 20:2712-2727
85. Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 2:239-260
86. Morris RGM (1989) Synaptic plasticity and learning: selective impairment of learning in rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 9:3040-3057 (Pubitemid 19260822)
87. Morris RG (2001) Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease. Philos Trans R Soc Lond Biol 356:1453-1465 (Pubitemid 32948870)
88. Morris RG, Baddeley AD (1988) Primary and working memory functioning in Alzheimer-type dementia. J Clin Exp Neuropsychol 10:279-296
89. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683 (Pubitemid 12096189)
90. Morris RG, Schenk 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
91. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7:217-227 (Pubitemid 27219858)
92. Nagao S, Kitazawa H (2008) Role of the cerebellum in the acquisition and consolidation of motor memory. Brain Nerve 60:783-790 (Pubitemid 352008323)
93. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, New York
94. Olton DS, Samuelson RJ (1976) Remembrance of places passed: spatial memory in rats. J Exp Psychol Anim Behav Process 2:97-116
95. Olton DS, Collison C, Werz MA (1977) Spatial memory and radial arm maze performance of rats. Learn Motiv 8:289-314
96. Pagonabarraga J, Kulisevsky J (2012) Cognitive impairment and dementia in Parkinson's disease. Neurobiol Dis 46:590-596
97. Paulesu E, Frith CD, Frackowiak RS (1993) The neural correlates of the verbal component of working memory. Nature 362:342-345 (Pubitemid 23101305)
98. Ramos JMJ (2000) Influence of the shape of the experimental room on spatial learning in rats. Physiol Behav 70:351-357
99. Ranganath C, Cohen MX, Dam C, D'Esposito M (2004) Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci 24:3917-3925 (Pubitemid 38544218)
100. Roberts WW, Dember WN, Brodwick M (1962) Alternation and exploration in rats with hippocampal lesions. J Comp Physiol Psychol 55:695-700
101. Rowe JB, Toni I, Josephs O, Frackowiak RSJ, Passingham RE (2000) The prefrontal cortex: response selection or maintenance with working memory? Science 288:1656-1660 (Pubitemid 30387434)
102. Salmon DP, Butters N (1995) Neurobiology of skill and habit learning. Curr Opin Neurobiol 5:184-190
103. Sanderson DJ, Bannerman DM (2012) The role of habituation in hippocampus-dependent spatial working memory tasks: evidence from GluA1 AMPA receptor subunit knockout mice. Hippocampus 22:981-994
104. Scolville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21
105. Smith EE, Jonides J (1997) Working memory: a view from neuroimaging. Cogn Psychol 33:5-42 (Pubitemid 127384736)
106. Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci USA 95:12061-12068 (Pubitemid 28460539)
107. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195-231
108. Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA 93:13515-13522 (Pubitemid 26424150)
109. Staddon JE (1984) Time and memory. Ann N Y Acad Sci 423:322-334 (Pubitemid 14122547)
110. Steele RJ, Morris RG (1999) Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9:118-136 (Pubitemid 29196956)
111. Stella F, Cerasti E, Si B, Jezek K, Treves A (2012) Self-organization of multiple spatial and context memories in the hippocampus. Neurosci Biobehav Rev 36:1609-1625
112. Stretton J, Thompson PJ (2012) Frontal lobe function in temporal lobe epilepsy. Epilepsy Res 8:1-13
113. Thompson E, Varela FJ (2001) Radical embodiment: neural dynamics and consciousness. Trends Cogn Sci 5:418-425 (Pubitemid 33064414)
114. Thopmson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16-43
115. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189-208
116. Tolman EC, Ritchie BF, Kalish D (1946) Studies in spatial learning. I. Orientation and the short-cut. J Exp Psychol 36:13-24
117. Tulving E (1972) Episodic and semantic memory. In: Tulving E, Donaldson W (eds) Organization of Memory. Academic Press, New York, pp 381-403
118. Tulving E (2002) Episodic memory: from mind to brain. Annu Rev Psychol 53:1-25
119. Van Dam D, Lenders G, De Deyn PP (2006) Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem 85:164-172 (Pubitemid 43247842)
120. van Os J, Kapur S (2009) Schizophrenia. Lancet 374:635-645
121. Wang SH, Morris RG (2010) Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61:49-79
122. Whishaw IQ (1989) Dissociating performance and learning deficits on spatial navigation tasks in rats subjected to cholinergic muscarinic blockade. Brain Res Bull 23:347-358 (Pubitemid 20008440)
123. Whishaw IQ, Cassel JC, Jarrad LE (1995) Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J Neurosci 15:5779-5788
124. Wolfer DP, Lipp HP (2000) Dissecting the behaviour of transgenic mice: is it the mutation, the genetic background, or the environment? Exp Physiol 85:627-634
125. Wolfer DP, Madani R, Valenti P, Lipp HP (2001) Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol Behav 73:745-753 (Pubitemid 32885563)
126. Zhou W, Crystal JD (2009) Evidence for remembering when events occurred in a rodent model of episodic memory. Proc Natl Acad Sci USA 101:9525-9529