The Effects of Aging on Memory for Sequentially Presented Objects in Rats

Behavioral Neuroscience

Volumn 123, Issue 6, 2009, Pages 1339-1345

  Hauser, Erin ^a   Tolentino, Jerlyn C ^a   Pirogovsky, Eva ^b   Weston, Erin ^a   Gilbert, Paul E ^a,b  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

aging; Fischer 344 Brown Norway rat; object memory; sequence; temporal order

Indexed keywords

AGE; AGED; AGING; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; COGNITION; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; LOCOMOTION; MALE; MEMORY DISORDER; MENTAL TASK; MOTIVATION; NEUROPSYCHOLOGICAL TEST; NONHUMAN; RAT; TASK PERFORMANCE;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; ATTENTION; BEHAVIOR, ANIMAL; EXPLORATORY BEHAVIOR; MALE; RATS; RATS, INBRED F344; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION; TIME FACTORS;

EID: 72249118043     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0017681     Document Type: Article

References (88)

1. Agster K.L., Fortin N.J., and Eichenbaum H. The hippocampus and disambiguation of overlapping sequences. Journal of Neuroscience 22 (2002) 5760-5768
2. Barker G.R., Bird F., Alexander V., and Warburton E.C. Recognition memory for objects, place, and temporal order: A disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. The Journal of Neuroscience 27 (2007) 2948-2957
3. Bizon J.L., LaSarge C.L., Montgomery K.S., McDermott A.N., Setlow B., and Griffith W.H. Spatial reference and working memory across the lifespan of male Fischer 344 rats. Neurobiology of Aging 30 (2009) 646-655
4. Brushfield A.M., Luu T.T., Callahan B.D., and Gilbert P.E. A comparison of discrimination and reversal learning for olfactory and visual stimuli in aged rats. Behavioral Neuroscience 122 (2008) 54-62
5. Cabeza R., Anderson N.D., Houle S., Mangels J.A., and Nyberg L. Age-related differences in neural activity during item and temporal-order memory retrieval: A positron emission tomography study. Journal of Cognitive Neuroscience 12 (2000) 197-206
6. Cabeza R., Mangels J., Nyberg L., Habib R., Houle S., and McIntosh A.R. Brain regions differentially involved in remembering what and when: A PET study. Neuron 19 (1997) 864-870
7. Chiba A.A., Kesner R.P., and Gibson C.J. Memory for temporal order of new and familiar spatial location sequences: Role of the medial prefrontal cortex. Learning and Memory 4 (1997) 311-317
8. Chiba A.A., Kesner R.P., and Reynolds A.M. Memory for spatial location as a function of temporal lag in rats: Role of hippocampus and medial prefrontal cortex. Behavioral and Neural Biology 61 (1994) 123-131
9. Coffey C.E., Wilkinson W.E., Parashos I.A., Soady S.A.R., Sullivan R.J., Patterson L.J., Figiel G.S., et al. Quantitative cerebral anatomy of the aging human brain: A cross-sectional study using magnetic resonance imaging. Neuropsychology 42 (1992) 527-536
10. Daum I., Graber S., Schugens M.M., and Mayes A.R. Memory dysfunction of the frontal type in normal ageing. Neuroreport 7 (1996) 2625-2628
11. Daum I., and Mayes A.R. Memory and executive function impairments after frontal or posterior cortex lesions. Behavioural Neurology 12 (2000) 161-173
12. DeCoteau W.E., and Kesner R.P. A double dissociation between the rat hippocampus and medial caudoputamen in processing two forms of knowledge. Behavioral Neuroscience 114 (2000) 1096-1108
13. Downes J.J., Mayes A.R., MacDonald C., and Hunkin N.M. Temporal order memory in patients with Korsakoff's syndrome and medial temporal amnesia. Neuropsychologia 40 (2002) 853-861
14. Driscoll I., Howard S.R., Stone J.C., Monfils M.H., Tomanek B., and Brooks W.M. The aging hippocampus: A multi-level analysis in the rat. Neuroscience 139 (2006) 1173-1185
15. Ekstrom A.D., and Bookheimer S.Y. Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain. Learning and Memory 14 (2007) 645-654
16. Ennaceur A., Neave N., and Aggleton J.P. Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Experimental Brain Research 113 (1997) 509-519
17. Ergorul C., and Eichenbaum H. Essential role of the hippocampal formation in rapid learning of higher-order sequential associations. Journal of Neuroscience 26 (2006) 4111-4117
18. Fabiani M., and Friedman D. Dissociations between memory for temporal order and recognition memory in aging. Neuropsychologia 35 (1997) 129-141
19. Fortin N.J., Agster K.L., and Eichenbaum H. Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience 5 (2002) 458-462
20. Fuster J.M. Executive frontal functions. Experimental Brain Research 133 (2000) 66-70
21. Fuster J.M. The prefrontal cortex-An update: Time is of the essence. Neuron 30 (2001) 319-333
22. Gallagher M., and Rapp P.R. The use of animal models to study the effects of aging on cognition. Annual Review of Psychology 48 (1997) 339-370
23. Gilbert P.E., and Kesner R.P. Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location. Behavioral Neuroscience 116 (2002) 63-71
24. Gilbert P.E., and Kesner R.P. Recognition memory for complex visual discriminations is influenced by stimulus interference in rodents with perirhinal cortex damage. Learning and Memory 10 (2003) 525-530
25. Gilbert P.E., Kesner R.P., and Lee I. Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1. Hippocampus 11 (2001) 626-636
26. Golomb J.D., Peelle J.E., Addis K.M., Kahana M.J., and Wingfield A. Effects of adult aging on utilization of temporal and semantic associations during free and serial recall. Memory & Cognition 36 (2008) 947-956
27. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., and Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14 (2001) 21-36
28. Hannesson D.K., Howland J.G., and Phillips A.G. Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats. Journal of Neuroscience 24 (2004) 4596-4604
29. Hannesson D.K., Vacca G., Howland J.G., and Phillips A.G. Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in rats. Behavioral Brain Research 153 (2004) 273-285
30. Hartman M., and Warren L.H. Explaining age differences in temporal working memory. Psychology and Aging 20 (2005) 645-656
31. Hoang L.T., and Kesner R.P. Dorsal hippocampus, CA3, and CA1 lesions disrupt temporal sequence completion. Behavioral Neuroscience 122 (2008) 9-15
32. Hoge J., and Kesner R.P. Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects. Neurobiology of Learning and Memory 88 (2007) 225-231
33. Hopkins R.O., Kesner R.P., and Goldstein M. Memory for novel and familiar spatial and linguistic temporal distance information in hypoxic subjects. Journal of the International Neuropsychological Society 1 (1995) 454-468
34. Hopkins R.O., Kesner R.P., and Goldstein M. Item and order recognition memory in subjects with hypoxic brain injury. Brain and Cognition 27 (1995) 180-201
35. Howland J.G., Harrison R.A., Hannesson D.K., and Phillips A.G. Ventral hippocampal involvement in temporal order, but not recognition, memory for spatial information. Hippocampus 18 (2008) 251-257
36. Hunsaker M.R., Fieldsted P.M., Rosenberg J.S., and Kesner R.P. Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. Behavioral Neuroscience 122 (2008) 643-650
37. Inoue M., and Mikami A. Prefrontal activity during serial probe reproduction task: Encoding, mnemonic, and retrieval processes. Journal of Physiology 95 (2006) 1008-1041
38. Jack Jr. C.R., Petersen R.C., Xu Y.C., Waring S.C., O'Brien P.C., Tangalos E.G., Smith G.E., et al. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology 49 (1997) 786-794
39. Jernigan T.L., Archibald S.L., Fennema-Notestine C., Gamst A.C., Stout J.C., Bonner J., and Hesselink J.R. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiology of Aging 22 (2001) 581-594
40. Kahana M.J., Howard M.W., Zaromb F., and Wingfield A. Age dissociates recency and lag recency effects in free recall. Journal of Experimental Psychology, Learning, Memory, and Cognition 28 (2002) 530-540
41. Kesner R.P., Gilbert P.E., and Barua L.A. The role of the hippocampus in memory for the temporal order of a sequence of odors. Behavioral Neuroscience 116 (2002) 286-290
42. Kesner R.P., Gilbert P.E., and Wallenstein G.V. Testing neural network models of memory with behavioral experiments. Current Opinion in Neurobiology 10 (2000) 260-265
43. Kesner R.P., Hopkins R.O., and Fineman B. Item and order dissociation in humans with prefrontal cortex damage. Neuropsychologia 32 (1994) 881-891
44. Kesner R.P., Hunsaker M.R., and Gilbert P.E. The role of CA1 in the acquisition of an object-trace-odor paired associate task. Behavioral Neuroscience 119 (2005) 781-786
45. Kesner R.P., and Novak J.M. Serial position curve in rats: Role of the dorsal hippocampus. Science 218 (1982) 173-175
46. Kessels R.P., Hobbel D., and Postma A. Aging, context memory and binding: A comparison of "what, where and when" in young and older adults. International Journal of Neuroscience 117 (2007) 795-810
47. Knutson K.M., Wood J.N., and Grafman J. Brain activation in processing temporal sequence: An fMRI study. NeuroImage 23 (2004) 1299-1307
48. Kraemer S., and Apfelbach R. Olfactory sensitivity, learning and cognition in young adult and aged male wistar rats. Physiological Behavior 81 (2004) 435-442
49. LaSarge C.L., Montgomery K.S., Tucker C., Slaton G.S., Griffith W.H., Setlow B., and Bizon J.L. Deficits across multiple cognitive domains in a subset of aged Fischer 344 rats. Neurobiology of Aging 28 (2007) 928-936
50. Lee I., Jerman T.S., and Kesner R.P. Disruption of delayed memory for a sequence of spatial locations following CA1-or CA3-lesions of the dorsal hippocampus. Neurobiology of Learning and Memory 84 (2005) 138-147
51. Lehn H., Steffenach H.A., van Strien N.M., Veltman D.J., Witter M.P., and Hayberg A.K. A specific role of the human hippocampus in recall of temporal sequences. Journal of Neuroscience 29 (2009) 3475-3484
52. Lewinsohn P.M., Zieler R.E., Libet J., Eyeberg S., and Nielson G. Short-term memory: A comparison between frontal and nonfrontal right- and left-hemisphere brain- damaged patients. Journal of Comparative and Physiological Psychology 81 (1972) 248-255
53. Luu T.T., Pirogovsky E., and Gilbert P.E. Age-related changes in contextual associative learning. Neurobiology of Learning and Memory 89 (2008) 81-85
54. Manns J.R., Howard M.W., and Eichenbaum H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 56 (2007) 530-540
55. Mayes A.R., Holdstock J.S., Isaac C.L., Montaldi D., Grigor J., Gummer A., Cariga P., et al. Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition. Hippocampus 14 (2004) 763-784
56. Milner B. Interhemispheric differences in the localization of psychological processes in man. Brain Medical Bulletin 27 (1971) 272-277
57. Milner B., Petrides M., and Smith M.L. Frontal lobes and the temporal organization of memory. Human Neurobiology 4 (1985) 137-142
58. Mitchell J.B., and Laiacona J. The medial prefrontal cortex and temporal memory: Tests using spontaneous exploratory behaviour in the rat. Behavioral Brain Research 97 (1998) 107-113
59. Naveh-Benjamin M. Coding of temporal order information: An automatic process?. Journal of Experimental Psychology: Learning, Memory, and Cognition 16 (1990) 117-126
60. Ninokura Y., Mushiake H., and Tanji J. Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. Journal of Neurophysiology 89 (2003) 2868-2873
61. Ninokura Y., Mushiake H., and Tanji J. Integration of temporal order and object information in the monkey lateral prefrontal cortex. Journal of Neurophysiology 91 (2004) 555-560
62. Nyberg L., McIntosh A.R., Cabeza R., Habib R., Houle S., and Tulving E. General and specific brain regions involved in encoding and retrieval of events: What, where, and when. Proceedings of the National Academy of Sciences, USA of the United States of America 93 (1996) 11280-11285
63. O'Donnell K.A., Rapp P.R., and Hof P.R. Preservation of prefrontal cortical volume in behaviorally characterized aged macaque monkeys. Experimental Neurology 160 (1999) 300-310
64. Old S.R., and Naveh-Benjamin M. Differential effects of age on item and associative measures of memory: A meta-analysis. Psychology and Aging 23 (2008) 104-118
65. Oztekin I., McElree B., Staresina B.P., and Davachi L. Working memory retrieval contributions of the left prefrontal cortex, the left posterior parietal cortex and the hippocampus. Journal of Cognitive Neuroscience 21 (2009) 581-593
66. Parkin A.J., Walter B.M., and Hunkin N.M. Relationships between normal aging, frontal lobe function, and memory for temporal and spatial information. Neuropsychology 9 (1995) 304-312
67. Peters A. Structural changes in the normally aging cerebral cortex of primates. Progress in Brain Research 136 (2002) 455-465
68. Peters A., and Rosene D.L. In aging, is it gray or white?. Journal of Comparative Neurology 462 (2003) 139-143
69. Peters A., Rosene D.L., Moss M.B., Kemper T.L., Abraham C.R., and Tigges J. Neurobiological bases of age-related cognitive decline in the rhesus monkey. Journal of Neuropathology and Experimental Neurology 55 (1996) 861-874
70. Petrides M., and Milner B. Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 20 (1982) 249-262
71. Raz N., Gunning-Dixon F.M., Head D., Dupuis J.H., and Acker J.D. Neuroanatomical correlates of cognitive aging: Evidence from structural magnetic resonance imaging. Neuropsychology 12 (1997) 95-114
72. Renteria A.F., Silbaugh B.C., Tolentino J.C., and Gilbert P.E. Age-related changes in conditioned flavor preference in rats. Behavioral Brain Research 188 (2008) 56-61
73. Robitsek R.J., Fortin N.J., Koh M.T., Gallagher M., and Eichenbaum H. Cognitive aging: A common decline of episodic recollection and spatial memory in rats. Journal of Neuroscience 28 (2008) 8945-8954
74. Roman F.S., Alescio-Lautier B., and Soumireu-Mourat B. Age-related learning and memory deficits in odor-reward association in rats. Neurobiology of Aging 17 (1996) 31-40
75. Rowe J.B., and Passingham R.E. Working memory for location and time: Activity in prefrontal area 46 relates to selection rather than maintenance in memory. Neuroimage 14 (2001) 77-86
76. Schmitter-Edgecombe M., and Simpson A.L. Effects of age and intentionality on content memory and temporal memory for performed activities. Aging, Neuropsychology, and Cognition 8 (2001) 81-97
77. Schoenbaum G., Nugent S., Saddoris M.P., and Gallagher M. Teaching old rats new tricks: Age related impairments in olfactory reversal learning. Neurobiology of Aging 23 (2002) 555-564
78. Sekuler R., McLaughlin C., Kahana M.J., Wingfield A., and Yotsumoto Y. Short-term visual recognition and temporal order memory are both well-preserved in aging. Psychology and Aging 21 (2006) 632-637
79. Shimamura A.P. Memory and the prefrontal cortex. Annals of the New York Academy of Sciences 769 (1995) 151-159
80. Shimamura A.P., Janowsky J.S., and Squire L.R. Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia 28 (1990) 803-813
81. Shukitt-Hale B., McEwen J.J., Szprengiel A., and Joseph J.A. Effect of age on the radial arm water maze-a test of spatial learning and memory. Neurobiology of Aging 25 (2004) 223-229
82. Small S.A., Tsai W.Y., DeLaPaz R., Mayeux R., and Stern Y. Imaging hippocampal function across the human life span: Is memory decline normal or not?. Annals of Neurology 51 (2002) 290-295
83. Smith D.E., Rapp P.R., McKay H.M., Roberts J.A., and Tuszynski M.H. Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. Journal of Neuroscience 24 (2004) 4373-4381
84. Solomon P.R., Beal M.F., and Pendlebury W.W. Age-related disruption of classical conditioning: A model systems approach to memory disorders. Neurobiology of Aging 9 (1988) 535-546
85. Szatkowska I., Szymanska O., and Grabowska A. The role of the human ventromedial prefrontal cortex in memory for contextual information. Neuroscience Letters 364 (2004) 71-75
86. Terry R.D., DeTeresa R., and Hansen L.A. Neocortical cell counts in normal human adult aging. Annals of Neurology 21 (1987) 530-539
87. Tulving E. Episodic memory: From mind to brain. Annual Reviews in Psychology 53 (2002) 1-25
88. Woodruff-Pak D.S., and Thompson R.F. Classical conditioning of the eyelid response in rabbits as a model system for the study of brain mechanisms of learning and memory in aging. Experimental Aging Research 11 (1985) 109-122