Multimodal sensory integration and concurrent navigation strategies for spatial cognition in real and artificial organisms

Journal of Integrative Neuroscience

Volumn 6, Issue 3, 2007, Pages 327-366

  Arleo, Angelo ^a   Rondi Reig, Laure ^b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

Behavioral strategies; Grid cells; Head direction cells; Hippocampal place cells; Multimodal information; Neuro mimetic models; Neuro robotics; Path integration; Spatial navigation

Indexed keywords

ARTICLE; BEHAVIOR; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; MATHEMATICAL ANALYSIS; ROBOTICS; SENSORY SYSTEM; SPATIAL DISCRIMINATION; SPATIAL MEMORY; TASK PERFORMANCE;

AFFERENT PATHWAYS; ANIMALS; COGNITION; HUMANS; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); NEURONS; ORIENTATION; SENSATION; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 35348885431     PISSN: 02196352     EISSN: None     Source Type: Journal    
DOI: 10.1142/S0219635207001593     Document Type: Article

References (171)

1. Abbott LF, Nelson SB, Synaptic plasticity: Taming the beast, Nat Neurosci 3 Suppl:1178-1183, 2000.
2. Arleo A, Spatial learning and navigation in neuromimetic systems, Modeling the Rat Hippocampus, Germany, Verlag-Dissertation, 2000.
3. Arleo A, Gerstner W, Spatial cognition and neuro-mimetic navigation: A model of hippocampal place cell activity, Biol Cybern 83 287-299, 2000.
4. Arleo A, Gerstner W, Spatial orientation in navigating agents: Modeling head-direction cells, Neurocomputing 38-40:1059-1065, 2001.
5. Arleo A, Gerstner W, Head direction cells and place cells in models for navigation and robotic applications, in Wiener SI, Taube JS (eds.), Head Direction Cells and the Neural Mechanisms of Spatial Orientation MIT Press, 2005.
6. Arleo, A, del R Millán J, Floreano D, Efficient learning of variable-resolution cognitive maps for autonomous indoor navigation, IEEE Trans Robot and Autom 15:990-1000, 1999.
7. Arleo A, Smeraldi F, Gerstner W, Cognitive navigation based on nonuniform Gabor space sampling, unsupervised growing networks, and reinforcement learning, IEEE Trans Neural Netw 15:639-652, 2004.
8. Barnes CA, Nadel L, Honig WK, Spatial memory deficit in senescent rats, Can J Psychol 34:29-39, 1980.
9. Barnes CA, Suster MS, Shen J, McNaughton BL, Multistability of cognitive maps in the hippocampus of old rats, Nature 388:272-275, 1997.
10. Bear MF, Bidirectional synaptic plasticity: From theory to reality, Philos Trans R Soc Lond B Biol Sci 358:649-655, 2003.
11. Bear MF, Malenka RC, Synaptic plasticity: LTP and LTD, Curr Opin Neurobiol 4:389-399, 1994.
12. Berthoz A, Viaud-Delmon I, Multisensory integration in spatial orientation, Curr Opin Neurobiol 9:708-712, 1999.
13. Best PJ, White AM, Minai A, Spatial processing in the brain: The activity of hippocampal place cells, Annu Rev Neurosci 24 459-486, 2001.
14. Biegler R, Morris RG, Landmark stability is a prerequisite for spatial but not discrimination learning, Nature 361:631-633, 1993.
15. Blair HT, Sharp PE, Anticipatory head direction signals in anterior thalamus: Evidence for a thalamocortical circuit that integrates angular head motion to compute head direction, J Neurosci 15 6260-6270, 1995.
16. Bostock E, Muller RU, Kubie JL, Experience-dependent modifications of hippocampal. place cell firing, Hippocampus 1:193-205, 1991.
17. Bower MR, Euston DR, McNaughton BL, Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements, J Neurosci 25:1313-1323, 2005.
18. Brooks RA, New approaches to robotics, Science 253 1227-1232, 1991.
19. Bures J, Fenton AA, Neurophysiology of Spatial Cognition, News Physiol Sci 15:233-240, 2000.
20. Burgess N, Jeffery KJ, O'Keefe J, Integrating hippocampal and parietal functions: A spatial point of view, The Hippocampal and Parietal Foundations of Spatial Cognition, Oxford University Press, pp. 3-29, 1999.
21. Burgess N, Maguire EA, O'Keefe J, The human hippocampus and spatial and episodic memory, Neuron 35:625-641, 2002.
22. Burgess N, Donnett JG, Jeffery KJ, O'Keefe J, Robotic and neuronal simulation of the hippocampus and rat navigation, Philos Trans R Soc Lond B Biol Sci 352:1535-1543, 1997.
23. Burguière E, Arleo A, Hojjati M, Elgersma Ǐ, De Zeeuro CI, Berthoz A, Rondi Reig L, Spatial navigation impairment in mice lacking cerebellar LTD: A motor adaptation deficit? Nat Neurosci 8 1292-1294, 2005.
24. Chang Q, Gold PE, Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats, J Neurosci 23:3001-3005, 2003.
25. Chavarriaga R, Spatial Learning and Navigation in the Rat: A Biomimetic Model, Swiss Federal Institute of Technology Lausanne, 2005.
26. Chavarriaga R, Strosslin T, Sheynikhovich D, Gerstner W, A computational model of parallel navigation systems in rodents, Neuroinformatics 3:223-241, 2005.
27. Chen LL, Lin LH, Green EJ, Barnes CA, Mc Naughtom BL, Head-direction cells in the rat posterior cortex. II. Contribution of visual and ideothetic information to the directional firing, Exp Brain Res 101:24-34, 1994a.
28. Chen LL, Lin LH, Green EJ, Barnes CA, Mc Naughton BL, Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation, Exp Brain Res 101:8-23, 1994b.
29. Cho YH, Giese KP, Tanila H, Silva AJ, Eichenbauon H, Abnormal hippocampal spatial representations in alphaCaMKIIT286A and CREBalphaDelta-mice, Science 279:867-869, 1998.
30. Collingridge GL, Kehl SJ, McLennan H, Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural, pathway of the rat hippocampus, J Physiol 334:33-46, 1983.
31. Cressant A, Muller RU, Poucet B, Failure of centrally placed objects to control the firing fields of hippocampal place cells, J Neurosci 17:2531-2542, 1997.
32. De Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, Van Alphen AM, Linden DJ, Obevdick J, Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex, Neuron 20:495-508, 1998.
33. Devan BD, White NM, Parallel information processing in the dorsal striatum: Relation to hippocampal function, J Neurosci 19 2789-2798, 1999.
34. Devan BD, Goad EH, Petri HL, Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze, Neurobiol Learn Mem 66:305-323, 1996.
35. Drai D, Kafkafi N, Benjamini Y, Elmer G, Golani I, Rats and mice share common ethologically relevant parameters of exploratory behavior, Behav Brain Res 125:133-140, 2001.
36. Dudchenko PA, Taube JS, Correlation between head direction cell activity and spatial behavior on a radial arm maze, Behav Neurosci 111 3-19, 1997.
37. Eichenbaum H, The hippocampus and declarative memory: Cognitive mechanisms and neural codes, Behav Brain Res 127:199-207, 2001.
38. Eichenbaum H, Cohen NJ, From Conditioning to Conscious Recollection New York, 2001.
39. Eichenbaum HE, Stewart C, Morris RGM, Hippocampal representation in spatial learning, J Neurosci 10:331-339, 1990.
40. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I, Cellular networks underlying human spatial navigation, Nature 425:184-188, 2003.
41. Elfes A, Sonar-based real-world mapping and navigation, IEEE J Robot and Autom 3:249-256, 1987.
42. Etienne AS, Jeffery KJ, Path integration in mammals, Hippocampus 14:180-192, 2004.
43. Etienne AS, Teroni E, Hurni C, Portenier V, The effec of a single light cue on homing behaviour of the golden hamster, Anim Behav, 39 17-41, 1990.
44. Etienne AS, Berlie J, Georgakopoulos J, Maurer R, Role of dead reckoning in navigation, in Healy S (ed.), Spatial Representation in Animals Oxford University Press, pp. 54-68, 1998a.
45. Etienne AS, Boulens V, Maurer R, Rowe T, Siegrist C, A brief view of known land-marks reorientates path integration in hamsters, Naturwissenschaften 87:494-498, 2000.
46. Etienne AS, Maurer R, Berlie J, Reverdin B, Rowe T, Georga Kopoulos J, Seguinot V, Navigation through vector addition, Nature 396 161-164, 1998b.
47. Fenton AA, Wesierska M, Kaminsky Y, Bures J, Both here and there: Simultaneous expression of autonomous spatial memories in rats, Proc Natl Acad Sci USA 95:11493-11498, 1998.
48. Fortin NJ, Agster KL, Eichenbaum HB, Critical role of the hippocampus in memory for sequences of events, Nat Neurosci 5:458-462, 2002.
49. Foster TC, Castro CA, McNaughton BL, Spatial selectivity of rat hippocampal neurons: Dependence on preparedness for movement, Science 244:1580-1582, 1989.
50. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB, Spatial representation in the entorhinal cortex, Science 305:1258-1264, 2004.
51. Gallistel CR, The Organization of Learning, MIT Press, Cambridge, 1990.
52. Gaussier P, Revel A, Banquet JP, Babeau V, From view cells and place cells to cognitive map learning: Processing stages of the hippocampal system, Biol Cybern 86:15-28, 2002.
53. Georgopoulos AP, Schwartz AB, Kettner RE, Neuronal population coding of movement direction, Science 233:1416-1419, 1986.
54. Girard B, Cuzin V, Guillot A, Gurney KN, Prescott TJ, A basal ganglia inspired model of action selection evaluated in a robotic survival task, J Integr Neurosci 2:179-200, 2003.
55. Golob EJ, Stackman RW, Wong AC, Taube JS, On the behavioral significance of head direction cells: Neural and behavioral dynamics during spatial memory tasks, Behav Neurosci 115:285-304, 2001.
56. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS, Cue control and head direction cells, Behav Neurosci 112:749-761, 1998.
57. Griffin AL, Eichenbaum H, Hasselmo ME, Spatial representations of hippocampal CA1 neurons are modulated by behavioral context in a hippocampus-dependent memory task, J Neurosci 27:2416-2423, 2007.
58. Griffin AS, Etienne AS, Updating the path integrator through a visual fix, Psychobiology 26:240-248, 1998.
59. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI, Microstructure of a spatial map in the entorhinal cortex, Nature 436:801-806, 2005.
60. Hamilton DA, Rosenfelt CS, Whishaw IQ, Sequential control of navigation by locale and taxon cues in the Morris water task, Behav Brain Res 154:385-397, 2004.
61. Haykin S, Neural Networks, A Comprehensive Foundation, NJd, MacMillan, Englewood Cliffs, 1994.
62. Hebb DO, The Organization of Behavior, John Wiley, New York, 1949.
63. Hermer L, Spelke ES, A geometric process for spatial reorientation in young children, Nature 370:57-59, 1994.
64. Hertz J, Krogh A, Palmer RG, Introduction to the Theory of Neural Computation, Addison-Wesley, Redwood City, CA, 1991.
65. Hill AJ, Best PJ, Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat, Exp Neurol 74:204-217, 1981.
66. Huerta PT, Sun LD, Wilson MA, Tonegawa S, Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons, Neuron 25 473-480, 2000.
67. Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD, Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice, J Neurosci 23 5945-5952, 2003.
68. Jarrard LE, Selective hippocampal lesions: Differential effects on performance by rats of a spatial task with preoperative versus postoperative training, J Comp Physiol Psychol 92:1119-1127, 1978.
69. Jeffery KJ, Learning of landmark stability and instability by hippocampal place cells, Neuropharmacology 37:677-687, 1998.
70. Jeffery KJ, O'Keefe JM, Learned interaction of visual and idiothetic cues in the control of place field orientation, Exp Brain Res 127:151-161, 1999.
71. Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L, Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task, Neuroreport 15 135-140, 2004.
72. Kentros C, Hargreaves E, Hawkins RD, Kandal ER, Shapiro M, Muller RV, Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor, blockade, Science 280:2121-2126, 1998.
73. Kim JJ, Baxter MG, Multiple brain-memory systems: The whole does not equal the sum of its parts, Trends Neurosci 24:324-330, 2001.
74. Knierim JJ, Kudrimoti HS, McNaughton BL, Place cells, head direction cells, and the learning of landmark stability, J Neurosci 15 1648-1659, 1995.
75. Knierim JJ, Kudrimoti HS, McNaughton BL, Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells, J Neurophysiol 80:425-446, 1998.
76. Korol DL, Role of estrogen in balancing contributions from multiple memory systems, Neurobiol Learn Mem 82:309-323, 2004.
77. Kuipers BJ, Byun YT, A robot exploration and mapping strategy based on a semantic hierarchy of spatial representations, Robot and Autonom Sys 8:47-63, 1991.
78. Lalonde R, Visuospatial abilities, in International Review of Neurobiology, Academic Press, New York, pp. 191-215, 1997.
79. Lavoie AM, Mizumori SJ, Spatial, movement- and reward-sensitive discharge by medial ventral striatum neurons of rats, Brain Res 638:157-168, 1994.
80. Learmonth AE, Newcombe NS, Huttenlocher J, Hermer L, Spelke ES, Toddlers' use of metric information and landmarks to reorient a geometric process for spatial reorientation in young children, J Exp Child Psychol 80:225-244, 2001.
81. Lee I, Kesner RP, Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory, Nat Neurosci 5:162-168, 2002.
82. Lenck-Santini PP, Save E, Poucet B, Place-cell firing does not depend on the direction of turn in a Y-maze alternation task, Eur J Neurosci 13:1055-1058, 2001a.
83. Lenck-Santini PP, Save E, Poucet B, Evidence for a relationship between place-cell spatial firing and spatial memory performance, Hippocampus 11:377-390, 2001b.
84. Lenck-Santini PP, Muller RU, Save E, Poucet B, Relationships between place cell firing fields and navigational decisions by rats, J Neurosci 22:9035-9047, 2002.
85. Lenck-Santini PP, Rivard B, Muller RU, Poucet B, Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial-changes in the environment, Hippocampus 15 356-369, 2005.
86. Malenka RC, Bear MF, LTP and LTD: An embarrassment of riches, Neuron 44:5-21, 2004.
87. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE, Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input. Hippocampus 4:410-421, 1994.
88. Marriott LK, Korol DL, Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning, Neurobiol Learn Mem 80:315-322, 2003.
89. Matthews DB, Ilgen M, White AM, Best PJ, Acute ethanol administration impairs spatial performance while facilitating nonspatial performance in rats, Neurobiol Learn Mem 72:169-179, 1999.
90. McDonald RJ, White NM, A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum, Behav Neurosci 107 3-22, 1993.
91. McDonald RJ, White NM, Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus, Behav Neural Biol 61:260-270, 1994.
92. McDonald RJ, White NM, Hippocampal and nonhippocampal contributions to place learning in rats, Behav Neurosci 109:579-593, 1995.
93. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA, Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice, Cell 87:1339-1349, 1996.
94. McNaughton BL, Chen LL, Markus EJ, Dead reckoning, landmark learning, and the sense of direction: A neurophysiological and computational hypothesis, J Cog Neurosci 3:190-202, 1991.
95. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB, Path integration and the neural basis of the "cognitive map," Nat Rev Neurosci 7:663-678, 2006.
96. Mittelstaedt H, Mittelstaedt ML, Homing by path integration, in Papi F, Wallraff HG (eds.), Avian Navigation, Springer, Berlin Heidelberg, 1982.
97. Mittelstaedt ML, Mittelstaedt H, Homing by path integration in the mammal, Naturewissenschaften 67:566-567, 1980.
98. Mizumori SJ, Williams JD, Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats, J Neurosci 13:4015-4028, 1993.
99. Molinari M, Petrosini L, Grammaldo LG, Spatial event processing, Int Rev Neurobiol 41:217-230, 1997.
100. Morris RG, Frey U, Hippocampal synaptic plasticity: Role in spatial learning or the automatic recording of attended experience, Philos Trans R Soc Lond B Biol Sci 352:1489-1503, 1997.
101. Morris RG, Garrud P, Rawlins JN, O'Keefe J, Place navigation impaired in rats with hippocampal lesions, Nature 297:681-683, 1982a.
102. Morris RG, Anderson E, Lynch GS, Baudry M, Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5, Nature 319 774-776, 1986a.
103. Morris RG, Schenk F, Tweedie F, Jarrard LE, Ibotenate lesions of hippocampus and/or subiculum: Dissociating components of allocentric spatial learning, Eur J Neurosci 2:1016-1028, 1990.
104. Morris RGM, Garrud P, Rawlins JNP, O'Keefe I, Place navigation impaired in rats with hippocampal lesions, Nature 297:681-683, 1982b.
105. Morris RGM, Anderson E, Lynch G, Baudry M, Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5, Nature 319 774-776, 1986b.
106. Muir GM, Taube JS, Head direction cell activity and behavior in a navigation task requiring a cognitive mapping strategy, Behav Brain Res 153:249-253, 2004.
107. Muller RU, Kubie JL, The effects of changes in ihe environment on the spatial firing of hippocampal complex-spike cells, J Neurosci 7 1951-1968, 1987.
108. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S, NMDA receptors, place cells and hippocampal spatial memory, Nat Rev Neurosci 5 361-372, 2004.
109. Nakazawa K, Sun LD, Quirk MC, Rondi Reig L, Wilson MA, Tonegawa S, Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience, Neuron 38:305-315, 2003.
110. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel ME, Sun LD, Kato A, Carr CA, Johnston D, Wilson MA, Requirement for hippocampal CA3 NMDA receptors in associative memory recall, Science 297:211-218, 2002.
111. O'Keefe J, Dostovsky J, The hippocampus as a spatial map, Preliminary evidence from unit activity in the freely-moving rat, Brain Res, 34:171-175, 1971.
112. O'Keefe J, Conway DH, Hippocampal place units in freely moving rats: Why they fire where they fire, Exp Brain Res 31:573-590, 1978.
113. O'Keefe J, Nadel L, The Hippocampus as a Cognitive Map, Clarendon Press, Oxford, 1978.
114. O'Keefe J, Speakman A, Single unit activity in the rat hippocampus during a spatial memory task, Exp Brain Res 68:1-27, 1987.
115. Packard MG, McGaugh JL, Inactivation of hippocampus or caudate nucleus with lidocaïne differentially affects expression of place and response learning, Neurobiol Learn Mem 65:65-72, 1996a.
116. Packard MG, McGaugh JL, Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning, Neurobiol Learn Mem 65:65-72, 1996.
117. Packard MG, Knowlton BJ, Learning and memory functions of the basal ganglia, Annu Rev Neurosci 25:563-593, 2002.
118. Passino E, Middei S, Restivo L, Bertaina-Anglade V, Ammassan-Teule M, Genetic approach to variability of memory systems: Analysis of place vs. response learning and fos-related expression in hippocampal and striatal areas of P57BL/6 and DBA/2 mice, Hippocampus 12:63-75, 2002.
119. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC, Storage of spatial information by the maintenance mechanism of LTP, Science 313:1141-1144, 2006.
120. Petrosini L, Molinari M, Dell'Anna ME, Cerebellar contribution to spatial event processing: Morris water maze and T-maze, Eur J Neurosci 9:1882-1896, 1996.
121. Quirk GJ, Muller RU, Kubie JL, The firing of hippocampal place cells in the dark depends on the rat's recent experience, J Neurosci 10 2008-2017, 1990.
122. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr, The positional firing properties of medial entorhinal neurons: Description and comparison with hippocampal place cells, J Neurosci 12:1945-1963, 1992.
123. Ranck JBJ, Head-direction cells in the deel cell layers of dorsal presubiculum in freely moving rats, Soc Neurosci Meet 10 599, 1984.
124. Redish AD, Beyond the Cognitive Map, From Place Cells to Episodic Memory, MIT Press, London, 1999.
125. Redish AD, Touretzky DS, The role of the hippocampus in solving the Morris water maze, Neural Comput 10:73-111, 1998.
126. Rondi-Reig L, Burguière E, Is the cerebellum ready for navigation? Prog Brain Res 148:199-212, 2005.
127. Rondi-Reig L, Caston J, Delhaye-Bouchaud N, Mariana J, Cerebellar functions: A behavioral neurogenetic perspective, in Neurobehavioral Genetics: Methods and Applications, CRC, 1999.
128. Rondi-Reig L, Libbey M, Eichenbaum H, Tonegawa S, CA1-specific N-methyl-D-aspartate receptor knockout mice are deficient in solving a nonspatial transverse patterning task, Proc Natl Acad Sci USA 98:3543-3548, 2001.
129. Rondi-Reig L, Le Marec N, Caston J, Mariani J, The role of climbing and parallel fibers inputs to cerebellar cortex in navigation, Behav Brain Res 132:11-18, 2002.
130. Rondi-Reig L, Petit G, Tobin C, Tonegawa S, Mariani J, Berthoz A, Impaired sequential-egocentric and allocentric memories in forebrain specific NMDA receptor knockout mice during a new task dissociating strategies of navigation, J Neurosci 26:4071-4081, 2006.
131. Salinas E, Abbott LF, Vector reconstruction from firing rates, J Comput Neurosci 1:89-107, 1994.
132. Samsanovich A, McNaughton B, Path integration and cognitive mapping in a continuous attractor neural network, J Neurosci 17 5900-5920, 1997.
133. Sanger TD, Optimal unsupervised learning in a single-layer linear feed forward neural network, Neural Networks 2:459-473, 1989.
134. Sargolini F, Fyhn M, Hafting T, Mc Naughton BL, Witter MP, Moser Mb, Moser EI, Conjunctive representation of position, direction, and velocity in entorhinal cortex, Science 312:758-762, 2006.
135. Save E, Poucet B, Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation, Behav Brain Res 109:195-206, 2000.
136. Save E, Poucet B, Foreman N, Buhot MC, Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation, Behav Neurosci 106 447-456, 1992.
137. Save E, Cressant A, Thinus-Blanc C, Poucet B, Spatial firing of hippocampal place cells in blind rats, J Neurosci 18 1818-1826, 1998.
138. Schultz W, Dayan P, Montague PR, A neural substrate of prediction and reward, Science 275:1593-1599, 1997.
139. Schölkopf B, Mallot HA, View-based cognitive mapping and path planning, Adaptive Behavior 3:311-348, 1995.
140. Sharp PE, Complimentary roles for hippocampal versus subicular/ entorhinal place cells in coding place, context, and events, Hippocampus 9:432-443, 1999.
141. Sharp PE, Kubie JL, Muller RU, Firing properties of hippocampal neurons in a visually symmetrical environment: Contributions of multiple sensory cues and mnemonic processes, J Neurosci 10:3093-3105, 1990.
142. Sharp PE, Tinkelman A, Cho J, Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: Implications for path integration in the head direction cell circuit, Behav Neurosci 115:571-588, 2001.
143. Stackman RW, Taube JS, Firing properties of head direction cells in the rat anterior thalamic nucleus: Dependence on vestibular input, J Neurosci 17:4349-4358, 1997.
144. Stackman RW, Taube JS, Firing properties of rat lateral mammillary single units: Head direction, head pitch, and angular head velocity, J Neurosci 18:9020-9037, 1998.
145. Steele RJ, Morris RG, Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5, Hippocampus 9:118-136, 1999.
146. Steffenach HA, Witter M, Moser MB, Moser EI, Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex, Neuron 45:301-313, 2005.
147. Taube JS, Head direction cells recorded in the anterior thalamic nuclei of freely moving rat, J Neurosci 15:70-86, 1995.
148. Taube JS, Head direction cells and the neurophysiological basis for a sense of direction, Prog Neurobiol 55:225-256, 1998.
149. Taube JS, Muller RU, Ranck Jr JB, Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations, J Neurosci 10:436-447, 1990.
150. Taube JS, Muller RU, Ranck JB, Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis, J Neurosci 10:420-435, 1990.
151. Thinus-Blanc C, Animal Spatial Cognition, World Scientific, Singapore, 1996.
152. Thrun S, Learning maps for indoor mobile robot navigation, Artif Intel 99:21-71, 1998.
153. Tolman EC, Cognitive maps in rats and men, Psychol Rev 55 189-208, 1948.
154. Trullier O, Meyer JA, Animat navigation using a cognitive graph, Biol Cybern 83:271-285, 2000.
155. Trullier O, Wiener SI, Berthoz A, Meyer JA, Biologically based artificial navigation systems: Review and prospects, Prog Neurobiol 51:483-544, 1997.
156. Tsien JZ, Huerta PT, Tonegawa S, The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory, Cell 87:1327-1338, 1996.
157. Vallar G, Lobel E, Galati G, Bevthoz A, Pizzamiglio L, Le Bihan D, A fronto-parietal system for computing the egocentric spatial frame of reference in humans, Exp Brain Res 124:281-286, 1999.
158. Whishaw IQ, Mittleman G, Visits to starts, routes, and places by rats (Rattus norvegicus) in swimming pool navigation tasks, J Comp Psychol 100:422-431, 1986.
159. White NM, McDonald RJ, Multiple parallel memory systems in the brain of the rat, Neurobiol Learn Mem 77:125-184, 2002.
160. Whitlock JR, Heynen AJ, Shuler MG, Bear MF, Learning induces long-term potentiation in the hippocampus, Science 313:1093-1097, 2006.
161. Wiener SI, Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task, J Neurosci 13 3802-3817, 1993.
162. Wiener SI, Arleo A, Persistent activity in limbic system neurons: Neurophysiological and modeling perspectives, J Physiol Paris 97:547-555, 2003.
163. Wiener SI, Taube JS, Head Direction Cells and the Neural Mechanisms of Spatial Orientation, MIT Press, 2005.
164. Wiener SI, Berthoz A, Zugaro MB, Multisensory processing in the elaboration of place and head direction responses by limbic system neurons, Brain Res Cogn Brain Res 14:75-90, 2002.
165. Wilson MA, McNaughton BL, Dynamics of the hippocampal ensemble code for space, Science 261:1055-1058, 1993.
166. Witter MP, Organization of the entorhinal-hippocampal system: A review of current anatomical data, Hippocampus 3:33-44, 1993.
167. Wood ER, Dudchenko PA, Eichenbaum H, Cellular correlates of behavior, Int Rev Neurobiol 45:293-312, 2001.
168. Wood ER, Dudchenko PA, Robitsek RJ, Erchembaum H, Hippocampal neurons encode information about different types of memory episodes occurring in the same location, Neuron 27:623-633, 2000.
169. Zugaro MB, Berthoz A, Wiener SI, Background but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons, J Neurosc 21:RC154(151-155), 2001.
170. Zugaro MB, Arleo A, Berthoz A, Wiener SI, Rapid spatial reorientation and head direction cells, J Neurosci 23:3478-3482, 2003.
171. Zugaro MB, Arleo A, Dejean C, Burguieve E, Khamassi M, Wiener SI, Rat anterodorsal thalamic head direction neurons depend upon dynamic visual signals to select anchoring landmark cues, Eur J Neurosci 20 530-536, 2004.