Space and context in the temporal cortex

Hippocampus

Volumn 17, Issue 9, 2007, Pages 813-825

  Bilkey, David K ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Hippocampus; Parasubiculum; Perirhinal cortex; Place cell; Presubiculum

Indexed keywords

BRAIN CORTEX; BRAIN MAPPING; DENTATE GYRUS; ENTORHINAL CORTEX; FIELD DENSITY MODEL; HIPPOCAMPUS; HUMAN; HYPOTHESIS; MODEL; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPATIAL MEMORY; SUBICULUM;

ANIMALS; BEHAVIOR, ANIMAL; HIPPOCAMPUS; MEMORY; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); NEURONS; SPACE PERCEPTION; SPATIAL BEHAVIOR; TEMPORAL LOBE;

EID: 34848893942     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20318     Document Type: Review

References (168)

1. Aggleton JP, Hunt PR, Rawlins JNP. 1986. The effects of hippocampal lesions on spatial and non- spatial tests of working memory. Behav Brain Res 19:133-146.
2. Aggleton JP, Kyd RJ, Bilkey DK. 2004. When is the perirhinal cortex necessary for the performance of spatial memory rasks? Neurosci Biobehav Rev 28:611-624.
3. Albertin SV, Mulder AB, Tabuchi E, Zugaro MB, Wiener SI. 2000. Lesions of the medial shell of the nucleus accumbens impair rats in finding larger rewards, but spare reward-seeking behavior. Behav Brain Res 117:173-183.
4. Amaral DG, Witter M. 1995. Hippocampal formation. In: Paxinos G, editor. The Rat Nervous System. San Diego CA: Academic Press. pp 443-493
5. Amaral DG, Witter MP. 1989. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31:571-591.
6. Anderson MI, jeffery KJ. 2003. Heterogeneous modulation of place cell firing by changes in context. J Neurosci 23:8827-8835.
7. Annett LE, McGregor A, Robbins TW. 1989. The effects of ibotenic acid lesions of the nucleus accumbens on spatial learning and extinction in the rat. Behav Brain Res 31:231-242.
8. Antle MC, Kriegsfeld LJ, Silver R. 2005. Signaling within the master clock of the brain: Localized activation of mitogen-activated protein kinase by gastrin-releasing peptide. J Neurosci 25:2447-2454.
9. Barry C, Lever C, Hayman R, Hartley T, Burton S, O'Keefe J, Jeffery K, Burgess N. 2006. The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci 17:71-97.
10. Bear MF, Abraham WC. 1996. Long-term depression in hippocampus. Annu Rev Neurosci 19:437-462.
11. Berridge KC. 1996. Food reward: Brain substrates of wanting and liking. Neurosci Biobehav Rev 20:1-25.
12. Bertoglio LJ, Joca SR, Guimaraes FS. 2006. Further evidence that anxiety and memory are regionally dissociated within the hippocampus. Behav Brain Res 175:183-188.
13. Bilkey DK, Clearwater J. 2005. The dynamic nature of spatial encoding in the hippocampus. Behav Neurosci 119:1533-1545.
14. Bilkey DK, Goddard GV. 1985. Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurons. Brain Res 361:99-106.
15. Bliss TVP, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (London) 232:331-356.
16. Bolte A, Goschke T. 2005. On the speed of intuition: Intuitive judgments of semantic coherence under different response deadlines. Mem Cognit 33:1248-1255.
17. Breese CR, Hampson RE, Deadwyler SA. 1989. Hippocampal place cells: Stereotypy and plasticity. J Neurosci 9:1097-1111.
18. Brown MW, Aggleton JP. 2001. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51-61.
19. Bucci DJ, Phillips RG, Burwell RD. 2000. Contributions of postrhinal and perirhinal cortex to contextual information processing. Behav Neurosci 114:882-894.
20. Bucci DJ, Saddoris MP, Burwell RD. 2002. Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behav Neurosci 116:479-488.
21. Buckley MJ. 2005. The role of the perirhinal cortex and hippocampus in learning, memory, and perception. QJ Exp Psychol B 58:246-268.
22. Buffalo EA, Bellgowan PS, Martin A. 2006. Distinct roles for medial temporal lobe structures in memory for objects and their locations. Learn Mem 13:638-643.
23. Burgess N, Hitch G. 2005. Computational models of working memory: Putting long-term memory into context. Trends Cogn Sci 9:535-541.
24. Burgess N, O'Keefe J. 1996. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus 6:749-762.
25. Burgess N, Jackson A, Hartley T, O'Keefe J. 2000. Predictions derived from modelling the hippocampal role in navigation. Biol Cybern 83:301-312.
26. Burwell RD, Amaral DG. 1998. Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391:293-321.
27. Burwell RD, Witter MP, Amaral DG. 1995. Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5:390-408.
28. Burwell RD, Bucci DJ, Sanborn MR, Jutras MJ. 2004a. Perirhinal and postrhinal contributions to remote memory for context. J Neurosci 24:11023-11028.
29. Burwell RD, Saddoris MP, Bucci DJ, Wiig KA. 2004b. Corticohippocampal contributions to spatial and contextual learning. J Neurosci 24:3826-3836.
30. Bussey TJ, Duck J, Muir JL, Aggleton JP. 2000. Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111:187-202.
31. Bussey TJ, Saksida LM, Murray EA. 2002. Perirhinal cortex resolves feature ambiguity in complex visual discriminations. Eur J Neurosci 15:365-374.
32. Bussey TJ, Saksida LM, Murray EA. 2006. Perirhinal cortex and feature-ambiguous discriminations. Learn Mem 13:103-105; author reply 106-107.
33. Caballero-Bleda M, Witter MP. 1993. Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: An anterograde tracing study in the rat. J Comp Neurol 328:115-129.
34. Caballero-Bleda M, Witter MP. 1994. Projections from the presubiculum and the parasubiculum to morphologically characterized entorhinal-hippocampal projection neurons in the rar. Exp Brain Res 101:93-108.
35. Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS. 2003. Hippocampal place cell instability after lesions of the head direction cell network. J Neurosci 23:9719-9731.
36. Clayton NS, Dickinson A. 1998. Episodic-like memory during cache recovery by scrub jays. Nature 395:272-274.
37. Colgan PW. 1989. Animal Motivation. London: Chapman and Hall.
38. Colombo M, Broadbent N. 2000. Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neurosci Biobehav Rev 24:465-484.
39. Cooper BG, Mizumori SJY. 1999. Retrosplenial cortex inactivation selectively impairs navigation in darkness. Neuroreport 10:625-630.
40. Cooper BG, Mizumori SJY. 2001. Temporary inactivation of the retrosplenial cortex causes a transient reorganization of spatial coding in the hippocampus. J Neurosci 21:3986-4001.
41. Cooper BG, Manka TF, Mizumori SJY. 2001. Finding your way in the dark: The retrosplenial cortex contributes to spatial memory and navigation without visual cues. Behav Neurosci 115:1012-1028.
42. Corodimas KP, LeDoux JE. 1995. Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: Contributions of contextual cues. Behav Neurosci 109:613-619.
43. Damasio AR. 1996. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond [Biol] 351:1413-1420.
44. Davies M, Machin PE, Sanderson DJ, Pearce JM, Aggleton JP. 2007. Neurotoxic lesions of the rat perirhinal and postrhinal cortices and their impact on biconditional visual discrimination tasks. Behav Brain Res 176:274-283.
45. Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, Horvath B, Gaskin FS, Nonaka N, Jaeger LB, Banks WA, Morley JE, Pinto S, Sherwin RS, Xu L, Yamada KA, Sleeman MW, Tschop MH, Horvath TL. 2006. Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 9:381-388.
46. Dijksterhuis A. 2004. Think different: The merits of unconscious thought in preference development and decision making. J Pers Soc Psychol 87:586-598.
47. Dutar P, Bassant MH, Senut MC, Lamour Y. 1995. The septohippocampal pathway: Structure and function of a central cholinergic system. Physiol Rev 75:393-427.
48. Eacott MJ, Machin PE, Gaffan EA. 2001. Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behav Brain Res 124:55-70.
49. 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.
50. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I. 2003. Cellular networks underlying human spatial navigation. Nature 425:184-188.
51. Fechner JH Jr, Buntin JD. 1989. Localization of prolactin binding sites in ring dove brain by quantitative autoradiography. Brain Res 487:245-254.
52. Floresco SB, Blaha CD, Yang CR, Phillips AG. 2001a. Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons. J Neurosci 21:6370-6376.
53. Floresco SB, Blaha CD, Yang CR, Phillips AG. 2001b. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: Cellular mechanisms of input selection. J Neurosci 21:2851-2860.
54. Freund TF, Antal M. 1988. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
55. Fyhn M, Molden S, Hollup S, Moser MB, Moser E. 2002. Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35:555-566.
56. Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B. 2004. Spatial representation in the entorhinal cortex. Science 305:1258-1264.
57. Gaffan D, Murray EA. 1992. Monkeys with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intervals and fail at matching to sample despite double sample presentations. Behav Neurosci 106:30-38.
58. Gao YJ, Ren WH, Zhang YQ, Zhao ZQ. 2004. Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats. Pain 110:343-353.
59. Goto Y, O'Donnell P. 2001. Synchronous activity in the hippocampus and nucleus accumbens in vivo. J Neurosci 21;RC131.
60. Griffin AL, Eichenbaum H, Hasselmo ME. 2007. Spatial representations of hippocampal CA1 neurons are modulated by behavioral context in a hippocampus-dependent memory task. J Neurosci 27:2416-2423.
61. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
62. Halberstadt JB, Wilson T. Reflections on conscious reflection. In: Rips L, Adler J, editors. Reasoning: Studies of Human Inference and Its Foundations. Cambridge: Cambridge University press (in press).
63. Hampton RR. 2001. Rhesus monkeys know when they remember. Proc Natl Acad Sci USA 98:5359-5362.
64. Harnad S. 1990. The symbol grounding problem. Physica D 42:335-346.
65. Hetherington PA, Shapiro ML. 1997. Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav Neurosci 111:20-34.
66. Hjorth-Simonsen A. 1971. Hippocampal efferents to the ipsilateral entorhinal area: An experimental study in the rat. J Comp Neurol 142:417-437.
67. Hjorth-Simonsen A. 1972. Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentate. J Comp Neurol 146:219-232.
68. Hjorth-Simonsen A, Jeune B. 1972. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 144:215-232.
69. Holland PC, Bouton ME. 1999. Hippocampus and context in classical conditioning. [Review] [75 refs]. Curr Opin Neurobiol 9:195-202.
70. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI. 2001. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21:1635-1644.
71. Holscher C. 2003. Time, space and hippocampal functions. Rev Neurosci 14:253-284.
72. Holscher C, Jacob W, Mallot HA. 2003. Reward modulates neuronal activity in the hippocampus of the rat. Behav Brain Res 142:181-191.
73. Jarrard LE. 1995. What does the hippocampus really do. Behav Brain Res 71:1-10.
74. Jarrard LE, Davidson TL, Bowring B. 2004. Functional differentiation within the medial temporal lobe in the rat. Hippocampus 14:434-449.
75. Jeffery KJ, Anderson MI. 2003. Dissociation of the geometric and contextual influences on place cells. Hippocampus 13:868-872.
76. Jeffery KJ, Gilbert A, Burton S, Strudwick A. 2003. Preserved performance in a hippocampal-dependent spatial task despite complete place cell remapping. Hippocampus 13:175-189.
77. Jeffery KJ, Anderson MI, Hayman R, Chakraborty S. 2004. A proposed architecture for the neural representation of spatial context. Neurosci Biobehav Rev 28:201-218.
78. Kennedy PJ, Shapiro ML. 2004. Retrieving memories via internal context requires the hippocampus. J Neurosci 24:6979-6985.
79. Knierim JJ. 2002. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci 22:6254-6264.
80. Kobayashi T, Nishijo H, Fukuda M, Bures J, Ono T. 1997. Task-dependent representations in rat hippocampal place neurons. J Neurophysiol 78:597-613.
81. Kobayashi T, Tran AH, Nishijo H, Ono T, Matsumoto G. 2003. Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats. Neuroscience 117:1025-1035.
82. Kohler C. 1985. Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504-522.
83. Lai Z, Roos P, Olsson Y, Larsson C, Nyberg F. 1992. Characterization of prolactin receptors in human choroid plexus. Neuroendocrinology 56:225-233.
84. LeDoux J. 1996. The Emotional Brain: The Mysterious Underpinnings of Emotional Life. New York: Simon and Schuster.
85. Lee I, Griffin AL, Zilli EA, Eichenbaum H, Hasselmo ME. 2006. Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron 51:639-650.
86. Lei ZM, Rao CV, Kornyei JL, Licht P, Hiatt ES. 1993. Novel expression of human chorionic gonadotropin/luteinizing hormone receptor gene in brain. Endocrinology 132:2262-2270.
87. Liu P, Bilkey DK. 1998a. Lesions of perirhinal cortex produce spatial memory deficits in the radial maze. Hippocampus 8:114-121.
88. Liu P, Bilkey DK. 1998b. Perirhinal cortex contributions to performance in the morris water maze. Behav Neurosci 112:304-315.
89. Liu P, Bilkey DK. 2001. The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav Neurosci 115:94-111.
90. Liu P, Jarrard LE, Bilkey DK. 2001. Excitotoxic lesions of the pre- and parasubiculum disrupt object recognition and spatial memory processes. Behav Neurosci 115:112-124.
91. Liu P, Jarrard LE, Bilkey DK. 2004. Excitotoxic lesions of the pre- and parasubiculum disrupt the place fields of hippocampal pyramidal cells. Hippocampus 14:107-116.
92. Lu X, Bilkey DK. 2002. Perirhinal cortex lesions affect place field size and may alter phase precession of hippocampal place cells. Soc Neurosci Abstracts 477:8.
93. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. 1995. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079-7094.
94. Martin PD. 2001. Locomotion towards a goal alters the synchronous firing of neurons recorded simultaneously in the subiculum and nucleus accumbens of rats. Behav Brain Res 124:19-28.
95. Martin PD, Ono T. 2000. Effects of reward anticipation, reward presentation, and spatial parameters on the firing of single neurons recorded in the subiculum and nucleus accumbens of freely moving rats. Behav Brain Res 116:23-38.
96. Meunier M, Bachevalier J, Mishkin M, Murray EA. 1993. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13:5418-5432.
97. Miller RM, Best PJ. 1980. Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex. Brain Res 194:311-323.
98. Mogenson GJ, Jones DL, Yim CY. 1980. From motivation to action: Functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97.
99. Moran JP, Dalrymple-Alford JC. 2003. Perirhinal cortex and anterior thalamic lesions: Comparative effects on learning and memory. Behav Neurosci 117:1326-1341.
100. Morris RGM. 1990. Does the hippocampus play a disproportionate role in spatial memory. Discuss Neurosci VI:39-45.
101. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
102. Muir GM, Bilkey DK. 2001. Instability in the place field location of hippocampal place cells after lesions centered on the perirhinal cortex. J Neurosci 21:4016-4025.
103. Muller RU. 1996. A quarter of a century of place cells. Neuron 17:813-822.
104. Muller RU, Kubie JL. 1987. The effects of changes in the environment on the spatial firing of hippocampal complex spike cells. J Neuroscience 7:1951-1968.
105. Muller RU, Stead M. 1996. Hippocampal place cells connected by Hebbian synapses can solve spatial problems. Hippocampus 6:709-719.
106. Muller RU, Kubie JL, Ranck JB. 1987. Spatial firing patterns of hippocampal complex spike cells in a fixed environment. J Neuroscience 7:1935-1950.
107. Mustafa A, Adem A, Roos P, Nyberg F. 1994a. Sex differences in binding of human growth hormone to rat brain. Neurosci Res 19:93-99.
108. Mustafa A, Nyberg F, Bogdanovic N, Islam A, Roos P, Adem A. 1994b. Somatogenic and lactogenic binding sites in rat brain and liver: Quantitative autoradiographic localization. Neurosci Res 20:257-263.
109. Naber PA, Caballero-Bleda M, Jorritsma-Byham B, Witter MP. 1997. Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport 8:2617-2621.
110. Nadel L, Willner J. 1980. Context and conditioning: A place for space. Physiol Psychol 8:218-228.
111. Norman G, Eacott MJ. 2004. Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behav Brain Res 148:79-91.
112. Norman G, Eacott MJ. 2005. Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav Neurosci 119:557-566.
113. O'Keefe J. 1999. Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352-364.
114. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381:425-428.
115. O'Keefe J, Conway DH. 1978. Hippocampal place units in the freely moving rat: Why they fire where they fire. Exp Brain Res 31:573-590.
116. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
117. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. Clarendon Press Oxford.
118. O'Keefe J, Speakman A. 1987. Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
119. Oomura Y, Hori N, Shiraishi T, Fukunaga K, Takeda H, Tsuji M, Matsumiya T, Ishibashi M, Aou S, Li XL, Kohno D, Uramura K, Sougawa H, Yada T, Wayner MJ, Sasaki K. 2006. Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 27:2738-2749.
120. Panksepp J. 1998. Affective Neuroscience: The Foundations of Human and Animal Emotions. New York: Oxford University Press.
121. Papp EC, Hajos N, Acsády L, Freund TF. 1999. Medial septal and median raphe innervation of vasoactive intestinal polypeptide-containing interneurons in the hippocampus. Neuroscience 90:369-382.
122. Poucet B, Lenck-Santini PP, Hok V, Save E, Banquet JP, Gaussier P, Muller RU. 2004. Spatial navigation and hippocampal place cell firing: The problem of goal encoding. Rev Neurosci 15:89-107.
123. Puryear CB, King M, Mizumori SJ. 2006. Specific changes in hippocampal spatial codes predict spatial working memory performance. Behav Brain Res 169:168-175.
124. Quirk GJ, Muller RU, Kubie JL, Ranck JB. 1992. The positional firing properties of medial entorhinal neurons - Description and comparison with hippocampal place cells. J Neurosci 12:1945-1963.
125. Ramos JM, Vaquero JM. 2005. The perirhinal cortex of the rat is necessary for spatial memory retention long after but not soon after learning. Physiol Behav 86:118-127.
126. Risold PY, Swanson LW. 1997. Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115-195.
127. Robinson TE, Berridge KC. 1993. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247-291.
128. Roesler R, Henriques JA, Schwartsmann G. 2006. Gastrin-releasing peptide receptor as a molecular target for psychiatric and neurological disorders. CNS Neurol Disord Drug Targets 5:197-204.
129. Sacchetti B, Lorenzini CA, Baldi E, Tassoni G, Bucherelli C. 1999. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J Neurosci 19:9570-9578.
130. Schultz W. 2004. Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr Opin Neurobiol 14:139-147.
131. Sharp PE. 2006. Subicular place cells generate the same "map" for different environments: Comparison with hippocampal cells. Behav Brain Res 174:206-214.
132. Shibata R, Mulder AB, Trullier O, Wiener SI. 2001. Position sensitivity in phasically discharging nucleus accumbens neurons of rats alternating between tasks requiring complementary types of spatial cues. Neuroscience 108:391-411.
133. Skaggs WE, McNaughton BL. 1998. Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J Neurosci 18:8455-8466.
134. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ. 1993. An information-theoretic approach to dechipering the hippocampal code. In: Hanson SJ, Cowan JD, Giles CL, editors. Advances in Neural Information Processing Systems. San Mateo, CA: Morgan Kaufmann. p 1030-1047.
135. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
136. Smith DM, Mizumori SJ. 2006a. Hippocampal place cells, context, and episodic memory. Hippocampus 16:716-729.
137. Smith DM, Mizumori SJ. 2006b. Learning-related development of context-specific neuronal responses to places and events: The hippocampal role in context processing. J Neurosci 26:3154-3163.
138. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: A mathematical model. Hippocampus 16:1026-1031.
139. Speakman A, O'Keefe J. 1990. Hippocampal complex spike cells do not change their place fields if the goal is moved within a cue controlled environment. Eur J Neurosci 2:544-555.
140. Spiers HJ, Maguire EA. 2006. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31:1826-1840.
141. Squire LR. 1992. Memory and the hippocampus: A synthesis from findings with rats, monkeys and humans. Psychol Rev 99:195-231.
142. Steffenach HA, Witter M, Moser MB, Moser EI. 2005. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313.
143. Steward O. 1976. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167:285-314.
144. Steward O, Scoville SA. 1976. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347-370.
145. Swanson LW, Cowan WM. 1977. An autoradiographic study of the organisation of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49-84.
146. Tabuchi E, Mulder AB, Wiener SI. 2000. Position and behavioral modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats. Hippocampus 10:717-728.
147. Tabuchi E, Mulder AB, Wiener SI. 2003. Reward value invariant place responses and reward site associated activity in hippocampal neurons of behaving rats. Hippocampus 13:117-132.
148. Tanila H, Shapiro ML, Eichenbaum H. 1997. Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613-623.
149. Taube JS. 1995. Place cells recorded in the parasubiculum of freely moving rats. Hippocampus 5:569-583.
150. Taube JS, Muller RU, Ranck JB Jr. 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420-435.
151. Taube JS, Kesslak JP, Cotman CW. 1992. Lesions of the rat postsubiculum impair performance on spatial tasks. Behav Neural Biol 57:131-143.
152. Thompson LT, Best PJ. 1990. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509:299-308.
153. Tolman EC, Honzik CH. 1930. Degrees of hunger, reward and non-reward on maze learning in the rat. Univ Calif Publ Psychol 4:241-256.
154. Tracy AL, Jarrard LE, Davidson TL. 2001. The hippocampus and motivation revisited: Appetite and activity. Behav Brain Res 127:13-23.
155. Trivedi MA, Coover GD. 2004. Lesions of the ventral hippocampus, but not the dorsal hippocampus, impair conditiored fear expression and inhibitory avoidance on the elevated T-maze. Neurobiol Learn Mem 81:172-184.
156. van Groen T, Wyss JM. 1990. The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227-243.
157. Vanderwolf CH. 2001. The hippocampus as an olfacto-motor mechanism: Were the classical anatomists right after all? Behav Brain Res 127:25-47.
158. Wallace DG, Gorny B, Whishaw IQ. 2002. Rats can track odors, other rats, and themselves: Implications for the study of spatial behavior. Behav Brain Res 131:185-192.
159. Wang D, Maler L. 1997. In vitro plasticity of the direct feedback pathway in the electrosensory system of Apteronotus leptorhynchus. J Neurophysiol 78:1882-1889.
160. Wiig KA, Bilkey DK. 1995. Lesions of rat perirhinal cortex exacerbate the memory deficir observed following damage to the fimbria-fornix. Behav Neurosci 109:620-630.
161. Wilson TD, Schooler JW. 1991. Thinking too much: Introspection can reduce the quality of preferences and decisions. J Pers Soc Psychol 60:181-192.
162. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bassey TJ. 2004. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Hererogeneity of function within the temporal lobe. J Neurosci 24:5901-5908.
163. Witter MP, Wouterlood FG, editors. 2002. The Parahippocampal Region: Organization and Role in Cognitive Function. Oxford: Oxford University Press.
164. Wong R. 2000. Motivation: A Biobehavioral Approach. Cambridge: Cambridge University Press.
165. Yang EJ, Nasipak BT, Kelley DB. 2007. Direct action of gonadotropin in brain integrates behavioral and reproductive functions. Proc Natl Acad Sci USA 104:2477-2482.
166. Young WS, Li J, Wersinger SR, Palkovits M. 2006. The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy. Neuroscience 143:1031-1039.
167. Zinyuk L, Kubik S, Kaminsky Y, Fenton AA, Bures J. 2000. Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames. Proc Natl Acad Sci USA 97:3771-3776.
168. Zola-Morgan S, Squire LR, Amaral ,D.G.and, Suzuki WA. 1989. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci 9:4355-4370.