Developing an animal model of human amnesia: The role of the hippocampus

Neuropsychologia

Volumn 48, Issue 8, 2010, Pages 2290-2302

  Kesner, Raymond P ^a   Goodrich Hunsaker, Naomi J ^b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hippocampus; Memory dysfunction; Sequence learning; Spatial and temporal processing

Indexed keywords

AMNESIA; ARTICLE; BRAIN DAMAGE; BRAIN FUNCTION; DISEASE MODEL; HIPPOCAMPUS; INFORMATION PROCESSING; LEARNING; MEDICAL RESEARCH; MEMORY DISORDER; METHODOLOGY; NONHUMAN; PERSONAL EXPERIENCE; RAT; SPATIAL DISCRIMINATION; SPATIAL MEMORY; SPECIES DIFFERENCE; TASK PERFORMANCE; TEMPORAL SUMMATION; TIME PERCEPTION; ANIMAL; BEHAVIOR; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMNESIA; ANIMALS; ASSOCIATION LEARNING; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; SERIAL LEARNING; SPATIAL BEHAVIOR;

EID: 77954174837     PISSN: 00283932     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2009.10.027     Document Type: Article

References (128)

1. Astur R.S., St Germain S.A., Baker E., Calhoun V., Pearlson G.D., Constable R.T. fMRI hippocampal activity during a virtual radial arm maze. Applied Psychophysiology and Biofeedback 2005, 30(3):307-317.
2. Banks W.P. Encoding and processing of symbolic information in comparative judgments. The psychology of learning and motivation: Advances in theory and research 1978, 101-159. Academic Press, New York. G.H. Bower (Ed.).
3. Barnes C.A. Spatial learning and memory processes: The search for their neurobiological mechanisms in the rat. Trends in Neuroscience 1988, 11(4):163-169.
4. Bower G., Black J., Turner T. Scripts in memory for text. Cognitive Psychology 1979, 11(2):177-220.
5. Brushfield, A.M., Kesner, R.P., & Gilbert, P.E. (2008). Role of the dentate gyrus in spatial pattern separation. Society for Neuroscience Abstract, 191.3.
6. Bunsey M., Eichenbaum H.B. Conservation of hippocampal memory function in rats and humans. Nature 1996, 379(6562):255-257.
7. Campbell C.B., Hodos W. The concept of homology and the evolution of the nervous system. Brain, Behavior and Evolution 1970, 3(5):353-367.
8. Chiba A.A., Kesner R.P., Jackson P. Two forms of spatial memory: A double dissociation between the parietal cortex and the hippocampus in the rat. Behavioral Neuroscience 2002, 116(5):874-883.
9. Chiba A.A., Kesner R.P., Reynolds A.M. Memory for spatial location as a function of temporal lag in rats: Role of hippocampus and medial prefrontal cortex. Behavioral Neural Biology 1994, 61(2):123-131.
10. Cho Y.H., Kesner R.P. Relational object association learning in rats with hippocampal lesions. Behavioural Brain Research 1995, 67(1):91-98.
11. Clark R.E., Squire L.R. Classical conditioning and brain systems: The role of awareness. Science 1998, 280(5360):77-81.
12. Cohen N.J., Squire L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science 1980, 210(4466):207-210.
13. Crane J., Milner B. What went where? Impaired object-location learning in patients with right hippocampal lesions. Hippocampus 2005, 15(2):216-231.
14. DeCoteau W.E., Kesner R.P. A double dissociation between the rat hippocampus and medial caudoputamen in processing two forms of knowledge. Behavioral Neuroscience 2000, 114(6):1096-1108.
15. Disterhoft J.F., Thompson L.T., Moyer J.R., Mogul D.J. Calcium-dependent after hyperpolarization and learning in young and aging hippocampus. Life Sciences 1996, 59(5-6):413-420.
16. Dudchenko P.A., Wood E.R., Eichenbaum H.B. Neurotoxic hippocampal lesions have no effect on odor span and little effect on odor recognition memory but produce significant impairments on spatial span, recognition, and alternation. Journal of Neuroscience 2000, 20(8):2964-2977.
17. Eichenbaum H.B. A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience 2000, 1(1):41-50.
18. Eichenbaum H.B., Cohen N.J. From conditioning to conscious recollection: Memory systems of the brain 2001, Oxford University Press, New York.
19. Eichenbaum H.B., Stewart C., Morris R.G. Hippocampal representation in place learning. Journal of Neuroscience 1990, 10(11):3531-3542.
20. Estes W.K. Memory for temporal information. Time, mind and behavior 1985, 151-168. Springer, New York. J.A. Michon, J.L. Jackson (Eds.).
21. Fortin N.J., Agster K.L., Eichenbaum H.B. Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience 2002, 5(5):458-462.
22. Gabrieli J.D., McGlinchey-Berroth R., Carrillo M.C., Gluck M.A., Cermak L.S., Disterhoft J.F. Intact delay-eyeblink classical conditioning in amnesia. Behavioral Neuroscience 1995, 109(5):819-827.
23. Gaffan D. Dissociated effects of perirhinal cortex ablation, fornix transection and amygdalectomy: Evidence for multiple memory systems in the primate temporal lobe. Experimental Brain Research 1994, 99(3):411-422.
24. Gaffan D., Harrison S. Place memory and scene memory: Effects of fornix transection in the monkey. Experimental Brain Research 1989, 74(1):202-212.
25. Gaykema R.P., van der Kuil J., Hersh L.B., Luiten P.G. Pattern of direct projections from the hippocampus to the medial septum-diagonal band complex: Anterograde tracing with Phaseolus vulgaris leucoagglutinin combined with immunohistochemistry of choline acetyltransferase. Neuroscience 1991, 43:349-360.
26. Gilbert P.E., Kesner R.P. Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location. Behavioral Neuroscience 2002, 116(1):63-71.
27. Gilbert P.E., Kesner R.P. Localization of function within the dorsal hippocampus: The role of the CA3 subregion in paired-associate learning. Behavioral Neuroscience 2003, 117(6):1385-1394.
28. Gilbert P.E., Kesner R.P. The role of the dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behavioural Brain Research 2006, 169(1):142-149.
29. Gilbert P.E., Kesner R.P., DeCoteau W.E. Memory for spatial location: Role of the hippocampus in mediating spatial pattern separation. Journal of Neuroscience 1998, 18(2):804-810.
30. Gilbert P.E., Kesner R.P., Lee I. Dissociating hippocampal subregions: Double dissociation between dentate gyrus and CA1. Hippocampus 2001, 11(6):626-636.
31. Goodrich-Hunsaker N.J., Gilbert P.E., Hopkins R.O. The role of the human hippocampus in odor-place associative memory. Chemical Senses 2009, 34:513-521.
32. Goodrich-Hunsaker, N. J., & Hopkins, R. O. (2008). Spatial deficits in a virtual radial arm maze in amnesic patients with hippocampal damage [Program No. 588.3. Neuroscience Meeting Planner]. Washington, DC: Society for Neuroscience.
33. Goodrich-Hunsaker N.J., Hunsaker M.R., Kesner R.P. Dissociating the role of the parietal cortex and dorsal hippocampus for spatial information processing. Behavioral Neuroscience 2005, 119(5):1307-1315.
34. Goodrich-Hunsaker N.J., Hunsaker M.R., Kesner R.P. The interactions and dissociations of the dorsal hippocampus subregions: How the dentate gyrus, CA3, and CA1 process spatial information. Behavioral Neuroscience 2008, 122(1):16-26.
35. Hartmann, H., Hopkins, R. O, & Kesner, R. P (unpublished observations). Impaired memory for spatial distance in amnesic patients with hippocampal damage.
36. Hopkins, R. O., & Kesner, R. P. (1993). Memory for temporal and spatial distances for new and previously learned geographical information in hypoxic subjects. Society for Neuroscience Abstracts: Vol. 19 (p. 1284). Washington, DC: Society for Neuroscience.
37. Hopkins, R. O. & Kesner, R.P. (unpublished observations). Memory for scripts: The role of the hippocampus in mediating memory for sequences of real world events in hypoxic subjects.
38. Hopkins R.O., Kesner R.P., Goldstein M. Memory for novel and familiar spatial and linguistic temporal distance information in hypoxic subjects. Journal of the International Neuropsychological Society 1995, 1(5):454-468.
39. Hopkins R.O., Myers C.E., Shohamy D., Grossman S., Gluck M. Impaired probabilistic category learning in hypoxic subjects with hippocampal damage. Neuropsychologia 2004, 42(4):524-535.
40. Hopkins, R. O., Pasker, M., & Kesner, R. P. (1995). Impaired spatial location object paired associate learning in hypoxic subjects. Society for Neuroscience Abstracts: Vol. 21 (p. 272). San Diego, CA: Society for Neuroscience.
41. Hopkins R.O., Waldram K., Kesner R.P. Sequences assessed by declarative and procedural tests of memory in amnesic patients with hippocampal damage. Neuropsychologia 2004, 42(14):1877-1886.
42. Huerta P.T., Sun L.D., Wilson M.A., Tonegawa S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 2000, 25(2):473-480.
43. Hunsaker M.R., Allan K.D., Kesner R.P. The role of dCA3 efferents via the fimbria in the acquisition of a delay-non-match to place task. Hippocampus 2007, 17:494-502.
44. Hunsaker M.R., Kesner R.P. Evaluating the differential roles of the dorsal dentate gyrus, dorsal CA3, and dorsal CA1 during a temporal ordering for spatial locations task. Hippocampus 2008, 18(9):955-964.
45. Hunsaker M.R., Tran G.T., Kesner R.P. A double dissociation of subcortical hippocampal efferents for encoding and consolidation/retrieval of spatial information. Hippocampus 2008, 18:699-709.
46. Hunt M.E., Kesner R.P., Evans R.B. Memory for spatial location: Functional dissociation of entorhinal cortex and hippocampus. Psychobiology 1994, 22(3):186-194.
47. Jarrard L.E. On the neural bases of the spatial mapping system: Hippocampus vs. hippocampal formation. Hippocampus 1991, 1(3):236-239.
48. Jarrard L.E. On the role of the hippocampus in learning and memory in the rat. Behavioral and Neural Biology 1993, 60(1):9-26.
49. Jarrard L., Davidson T. Acquisition of concurrent conditional discriminations in rats with ibotenate lesions of hippocampus and of subiculum. Psychobiology 1990, 18:68-73.
50. Jenkins T.A., Amin E., Pearce J.M., Brown M.W., Aggleton J.P. Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: A c-fos expression study. Neuroscience 2004, 124(1):43-52.
51. Jerman T., Kesner R.P., Hunsaker M.R. Disconnection analysis of CA3 and DG in mediating encoding but not retrieval in a spatial maze learning task. Learning & Memory 2006, 13:458-464.
52. Kesner R.P. Neural mediation of memory for time: Role of the hippocampus and medial prefrontal cortex. Psychonomic Bulletin and Review 1998, 5:585-596.
53. Kesner R.P. Neurobiological views of memory. Neurobiology of learning and memory 1998, 361-416. Academic Press, San Diego, CA. J.L. Martinez, R.P. Kesner (Eds.).
54. Kesner R.P. Neurobiology views of memory. The neurobiology of learning and memory 2007, 271-304. Academic Press, San Diego, CA. 2nd ed. R.P. Kesner, J.L. Martinez (Eds.).
55. Kesner R.P., Gilbert P.E., Barua L. The role of the hippocampus in memory for the temporal order of a sequence of odors. Behavioral Neuroscience 2002, 116(2):286-290.
56. Kesner R.P., Hopkins R.O. Short-term memory for duration and distance in humans: Role of the hippocampus. Neuropsychology 2001, 15(1):58-68.
57. Kesner R.P., Hunsaker M.R., Gilbert P.E. The role of CA1 in the acquisition of an object-trace-odor paired associate task. Behavioral Neuroscience 2005, 119(3):781-786.
58. Kesner R.P., Hunsaker M.R., Warthen M.W. The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats. Behavioral Neuroscience 2008, 122(6):1217-1225.
59. King J., Burgess N., Hartley T., Vargha-Khadem F., O'Keefe J. Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 2002, 12(6):811-820.
60. King J., Trinkler I., Hartley T., Vargha-Khadem F., Burgess N. The hippocampal role in spatial memory and the familiarity-recollection distinction: A case study. Neuropsychology 2004, 18(3):405-417.
61. Kumaran D., Hassabis D., Spiers H.J., Vann S.D., Vargha-Khadem F., Maguire E.A. Impaired spatial and non-spatial configural learning in patients with hippocampal pathology. Neuropsychologia 2007, 45(12):2699-2711.
62. Lee I., Hunsaker M.R., Kesner R.P. The role of hippocampal subregions in detecting spatial novelty. Behavioral Neuroscience 2005, 119(1):145-153.
63. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience 2003, 23(4):1517-1523.
64. 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.
65. Lee I., Solivan F. The roles of the medial prefrontal cortex and hippocampus in a spatial paired-association task. Learning & Memory 2008, 15(5):357-367.
66. Li H., Matsumoto K., Watanabe H. Different effects of unilateral and bilateral hippocampal lesions in rats on the performance of radial maze and odor-paired associate tasks. Brain Research Bulletin 1999, 48(1):113-119.
67. Long J.M., Kesner R.P. The effects of dorsal versus ventral hippocampal, total hippocampal, and parietal cortex lesions on memory for allocentric distance in rats. Behavioral Neuroscience 1996, 110(5):922-932.
68. Madsen J., Kesner R.P. The temporal-distance effect in subjects with dementia of the Alzheimer type. Alzheimer Disease and Associated Disorders 1995, 9(2):94-100.
69. Maguire E.A., Burke T., Phillips J., Staunton H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 1996, 34(10):993-1001.
70. Manns J., Hopkins R.O., Reed J.M., Kitchener E.G., Squire L.R. Recognition memory and the human hippocampus. Neuron 2003, 37(1):171-180.
71. Manns J., Hopkins R.O., Squire L.R. Semantic memory and the human hippocampus. Neuron 2003, 38(1):127-133.
72. Marr D. Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 1971, 262(841):23-81.
73. McDonald R.J., White N.M. Hippocampal and nonhippocampal contributions to place learning in rats. Behavioral Neuroscience 1995, 109(4):579-593.
74. McGlinchey-Berroth R., Carrillo M.C., Gabrieli J.D., Brawn C.M., Disterhoft J.F. Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience 1997, 111(5):873-882.
75. McNaughton B.L., Nadel L. Hebb-Marr networks and the neurobiological representation of action in space. Neuroscience and connectionist theory 1989, 1-63. Erlbaum, Hillsdale, NJ. M.A. Gluck, D.E. Rumelhart (Eds.).
76. Mikulka P.J., Freeman F.G. The effects of reinforcement delay and hippocampal lesions on the acquisition of a choice response. Behavioral Biology 1975, 15(4):473-477.
77. Mizumori S.J. A context for hippocampal place cells during learning. Hippocampal place fields: Relevance to learning and memory 2008, 16-43. Oxford University Press, New York. S.J. Mizumori (Ed.).
78. Morris R.G. Theories of hippocampal function. The hippocampus book 2007, 581-713. Oxford University Press, New York. P. Andersen, R.G. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
79. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
80. Moses S., Ryan J.D. A comparison and evaluation of the predictions of relational and conjunctive accounts of hippocampal function. Hippocampus 2006, 16(1):43-65.
81. Moyer J.R., Deyo R.A., Disterhoft J.F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience 1990, 104(2):243-252.
82. Murray E.A., Gaffan D., Mishkin M. Neural substrates of visual stimulus-stimulus association in rhesus monkeys. Journal of Neuroscience 1993, 13(10):4549-4561.
83. Mutter S.A., Howard J.H., Howard D.V. Serial pattern learning after head injury. Journal of Clinical and Experimental Neuropsychology 1994, 16(2):271-288.
84. Myers C.E., Scharfman H.E. A role for hilar cells in pattern separation in the dentate gyrus: A computational approach. Hippocampus 2009, 19(4):321-337.
85. Nadel L., Hardt O. The spatial brain. Neuropsychology 2004, 18(3):473-476.
86. Nissen M., Bullemer P. Attentional requirements of learning: Evidence from performance measures. Cognitive Psychology 1987, 19(1):1-32.
87. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research 1971, 34(1):171-175.
88. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press, Oxford.
89. O'Reilly R.C., McClelland J.L. Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus 1994, 4(6):661-682.
90. Okaichi H., Oshima Y. Choice behavior of hippocampectomized rats in the radial arm maze. Psychobiology 1990, 18(4):416-421.
91. Olton D., Becker J., Handelmann G. Hippocampus, space and memory. Behavioral and Brain Sciences 1979, 2:313-365.
92. Otto T., Eichenbaum H.B. Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: Evidence for hippocampal processing in recognition memory. Hippocampus 1992, 2(3):323-334.
93. Owen A.M., Sahakian B.J., Semple J., Polkey C.E., Robbins T.W. Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 1995, 33(1):1-24.
94. Poucet B. Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. Behavioral Neuroscience 1989, 103(5):1009-1016.
95. Preston A.R., Wagner A.D. The medial temporal lobe and memory. Neurobiology of learning and memory 2007, 305-337. Academic Press, San Diego, CA. 2 ed. R.P. Kesner, J.L. Martinez (Eds.).
96. Raisman G., Cowan M.W., Powell T.P.S. An experimental analysis of the efferent projection of the hippocampus. Brain 1966, 89:83-108.
97. Rawlins J.N. Associations across time: The hippocampus as a temporary memory store. Behavioral and Brain Sciences 1987, 10(1):154-160.
98. Reber P.J., Squire L.R. Parallel brain systems for learning with and without awareness. Learning & Memory 1994, 1(4):217-229.
99. Reber P.J., Squire L.R. Encapsulation of implicit and explicit memory in sequence learning. Journal of Cognitive Neuroscience 1998, 10(2):248-263.
100. Rolls E.T. A theory of hippocampal function in memory. Hippocampus 1996, 6(6):601-620.
101. Rolls E.T. An attractor network in the hippocampus: Theory and neurophysiology. Learning & Memory 2007, 14(11):714-731.
102. 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.
103. Rudy J.W., Sutherland R.J. Configural association theory and the hippocampal formation: An appraisal and reconfiguration. Hippocampus 1995, 5(5):375-389.
104. Save E., Poucet B. Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behavioural Brain Research 2000, 109(2):195-206.
105. Schacter L.L. Implicit memory: History and current status. Journal of Experimental Psychology: Learning, Memory, and Cognition 1987, 13:501-518.
106. Schank R.C., Abelson R.P. Scripts, plans, goals, and understanding: An inquiry into human knowledge structures 1977, Lawrence Erlbaum, New York.
107. Scoville W., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry 1957, 20(1):11-21.
108. Shapiro M.L., Olton D.S. Hippocampal function and interference. Memory systems 1994, 141-146. MIT Press, Cambridge, MA. D.L. Schacter, E. Tulving (Eds.).
109. Shrager Y., Bayley P.J., Bontempi B., Hopkins R.O., Squire L.R. Spatial memory and the human hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(8):2961-2966.
110. Shrager Y., Kirwan C.B., Squire L.R. Neural basis of the cognitive map: Path integration does not require hippocampus or entorhinal cortex. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(33):12034-12038.
111. Smith M.L., Milner B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 1981, 19(6):781-793.
112. Smith M.L., Milner B. Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting?. Neuropsychologia 1989, 27(1):71-81.
113. Spiers H.J., Burgess N., Maguire E.A., Baxendale S.A., Hartley T., Thompson P.J., et al. Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 2001, 124(Pt 12):2476-2489.
114. Squire L.R. Declarative and nondeclarative memory: Multiple brain systems supporting learning and memory. Memory systems 1994 1994, 203-231. MIT Press, Cambridge, MA. D.L. Schacter, E. Tulving (Eds.).
115. Stepankova K., Fenton A.A., Pastalkova E., Kalina M., Bohbot V.D. Object-location memory impairment in patients with thermal lesions to the right or left hippocampus. Neuropsychologia 2004, 42(8):1017-1028.
116. Swanson L.W., Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation of the rat. Journal of Comparative Neurology 1977, 172:49-84.
117. Swanson L.W., Cowan W.M. The connections of the septal region in the rat. Journal of Comparative Neurology 1979, 186:621-656.
118. Sziklas V., Lebel S., Petrides M. Conditional associative learning and the hippocampal system. Hippocampus 1998, 8(2):131-137.
119. Sziklas V., Petrides M., Leri F. The effects of lesions to the mammillary region and the hippocampus on conditional associative learning by rats. European Journal of Neuroscience 1996, 8(1):106-115.
120. Tolman E.C. Cognitive maps in rats and men. Psychological Review 1948, 55(4):189-208.
121. Tulving E. Elements of episodic memory 1983, Clarendon Press, Oxford, UK.
122. 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, 17:977-987.
123. Vann S.D., Aggleton J.P. The mammillary bodies: Two memory systems in one?. Nature Review Neuroscience 2004, 5:35-44.
124. Walker J.A., Olton D.S. Spatial memory deficit following fimbria-fornix lesions: Independent of time for stimulus processing. Physiology & Behavior 1979, 23(1):11-15.
125. Weiss C., Bouwmeester H., Power J.M., Disterhoft J.F. Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behavioural Brain Research 1999, 99(2):123-132.
126. Wyss X., Swanson I.W., Cowan W.M. The organization of the fimbria, dorsal fornix, and ventral hippocampal commissure in the rat. Anatomy and Embryology 1980, 138:303-316.
127. Wood E., Agster K.L., Eichenbaum H.B. One-trial odor-reward association: A form of event memory not dependent on hippocampal function. Behavioral Neuroscience 2004, 118(3):526-539.
128. Woodruff-Pak D.S. Eyeblink classical conditioning in H.M.: Delay and trace paradigms. Behavioral Neuroscience 1993, 107(6):911-925.