The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions

Neuron

Volumn 88, Issue 1, 2015, Pages 64-77

  Chersi, Fabian ^a   Burgess, Neil ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION; BRAIN REGION; COGNITION; CORPUS STRIATUM; EPISODIC MEMORY; EXPERIMENTAL STUDY; HIPPOCAMPUS; HUMAN; IMAGERY; LEARNING; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MEDIAL PREFRONTAL CORTEX; MENTAL PERFORMANCE; NERVE CELL; NEUROSCIENCE; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; SENSORY NERVE; SPATIAL LEARNING; SPATIAL ORIENTATION; BRAIN; IMAGINATION; NEOSTRIATUM; PHYSIOLOGY; PREFRONTAL CORTEX;

BRAIN; COGNITION; HIPPOCAMPUS; HUMANS; IMAGINATION; LEARNING; MEMORY, EPISODIC; NEOSTRIATUM; PREFRONTAL CORTEX; REINFORCEMENT (PSYCHOLOGY); SPATIAL NAVIGATION;

EID: 84943267892     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.09.021     Document Type: Review

References (172)

1. Andersen R.A. Encoding of intention and spatial location in the posterior parietal cortex. Cereb. Cortex 1995, 5:457-469.
2. Balleine B.W., Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 1998, 37:407-419.
3. Barnes T.D., Kubota Y., Hu D., Jin D.Z., Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 2005, 437:1158-1161.
4. Barraclough D.J., Conroy M.L., Lee D. Prefrontal cortex and decision making in a mixed-strategy game. Nat. Neurosci. 2004, 7:404-410.
5. Barry C., Burgess N. Learning in a geometric model of place cell firing. Hippocampus 2007, 17:786-800.
6. Barry C., Lever C., Hayman R., Hartley T., Burton S., O'Keefe J., Jeffery K., Burgess N. The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 2006, 17:71-97.
7. Barry C., Hayman R., Burgess N., Jeffery K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 2007, 10:682-684.
8. Barry C., Bush D., O'Keefe J., Burgess N. Models of grid cells and theta oscillations. Nature 2012, 488:E1-E2. discussion E2-E3.
9. Baumann O., Mattingley J.B. Functional topography of primary emotion processing in the human cerebellum. Neuroimage 2012, 61:805-811.
10. Benoit R.G., Szpunar K.K., Schacter D.L. Ventromedial prefrontal cortex supports affective future simulation by integrating distributed knowledge. Proc. Natl. Acad. Sci. USA 2014, 111:16550-16555.
11. Berendse H.W., Galis-de Graaf Y., Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 1992, 316:314-347.
12. Berke J.D., Breck J.T., Eichenbaum H. Striatal versus hippocampal representations during win-stay maze performance. J. Neurophysiol. 2009, 101:1575-1587.
13. Bisiach E., Luzzatti C. Unilateral neglect of representational space. Cortex 1978, 14:129-133.
14. Blum K.I., Abbott L.F. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 1996, 8:85-93.
15. Boccara C.N., Sargolini F., Thoresen V.H., Solstad T., Witter M.P., Moser E.I., Moser M.-B. Grid cells in pre- and parasubiculum. Nat. Neurosci. 2010, 13:987-994.
16. Bornstein A.M., Daw N.D. Multiplicity of control in the basal ganglia: computational roles of striatal subregions. Curr. Opin. Neurobiol. 2011, 21:374-380.
17. Brown M.A., Sharp P.E. Simulation of spatial learning in the Morris water maze by a neural network model of the hippocampal formation and nucleus accumbens. Hippocampus 1995, 5:171-188.
18. Burak Y., Fiete I.R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 2009, 5:e1000291.
19. Burgess N. The 2014 Nobel Prize in Physiology or Medicine: a spatial model for cognitive neuroscience. Neuron 2014, 84:1120-1125.
20. Burgess N., O'Keefe J. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus 1996, 6:749-762.
21. Burgess N., Recce M., O'Keefe J. A model of hippocampal function. Neural Netw. 1994, 7:1065-1081.
22. Burgess N., Becker S., King J.A., O'Keefe J. Memory for events and their spatial context: models and experiments. Phil. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1493-1503.
23. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35:625-641.
24. Burton B.G., Hok V., Save E., Poucet B. Lesion of the ventral and intermediate hippocampus abolishes anticipatory activity in the medial prefrontal cortex of the rat. Behav. Brain Res. 2009, 199:222-234.
25. Bush D., Barry C., Manson D., Burgess N. Using grid cells for navigation. Neuron 2015, 87:507-520.
26. Byrne P., Becker S., Burgess N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 2007, 114:340-375.
27. Carpenter F., Manson D., Jeffery K., Burgess N., Barry C. Grid cells form a global representation of connected environments. Curr. Biol. 2015, 25:1176-1182.
28. Chersi F., Pezzulo G. Using hippocampal-striatal loops for spatial navigation and goal-directed decision-making. Cogn. Process. 2012, 13(Suppl 1):S125-S129.
29. Chersi F., Donnarumma F., Pezzulo G. Mental imagery in the navigation domain: a computational model of sensory-motor simulation mechanisms. Adapt. Behav. 2013, 21:251-262.
30. Clark B.J., Harris M.J., Taube J.S. Control of anterodorsal thalamic head direction cells by environmental boundaries: comparison with conflicting distal landmarks. Hippocampus 2012, 22:172-187.
31. Cohen N.J., Eichenbaum H. Memory, Amnesia, and the Hippocampal System 1993, MIT Press.
32. Cohen J.S., Laroche J.P., Beharry E. Response perseveration in the hippocampal lesioned rat. Psychon. Sci. 1971, 23:221-223.
33. Conklin J., Eliasmith C. A controlled attractor network model of path integration in the rat. J. Comput. Neurosci. 2005, 18:183-203.
34. Cressant A., Muller R.U., Poucet B. Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 1997, 17:2531-2542.
35. Daw N.D., Niv Y., Dayan P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat. Neurosci. 2005, 8:1704-1711.
36. Dayan P. Goal-directed control and its antipodes. Neural Netw. 2009, 22:213-219.
37. Derdikman D., Whitlock J.R., Tsao A., Fyhn M., Hafting T., Moser M.-B., Moser E.I. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 2009, 12:1325-1332.
38. Dhindsa K., Drobinin V., King J., Hall G.B., Burgess N., Becker S. Examining the role of the temporo-parietal network in memory, imagery, and viewpoint transformations. Front. Hum. Neurosci. 2014, 8:709. 10.3389/fnhum.2014.00709.
39. Diba K., Buzsáki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 2007, 10:1241-1242.
40. Doeller C.F., Burgess N. Distinct error-correcting and incidental learning of location relative to landmarks and boundaries. Proc. Natl. Acad. Sci. USA 2008, 105:5909-5914.
41. Doeller C.F., King J.A., Burgess N. Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc. Natl. Acad. Sci. USA 2008, 105:5915-5920.
42. Doeller C.F., Barry C., Burgess N. Evidence for grid cells in a human memory network. Nature 2010, 463:657-661.
43. Dollé L., Sheynikhovich D., Girard B., Chavarriaga R., Guillot A. Path planning versus cue responding: a bio-inspired model of switching between navigation strategies. Biol. Cybern. 2010, 103:299-317.
44. Dupret D., O'Neill J., Pleydell-Bouverie B., Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 2010, 13:995-1002.
45. Ekstrom A.D., Kahana M.J., Caplan J.B., Fields T.A., Isham E.A., Newman E.L., Fried I. Cellular networks underlying human spatial navigation. Nature 2003, 425:184-188.
46. FitzGerald T.H., Schwartenbeck P., Dolan R.J. Reward-related activity in ventral striatum is action contingent and modulated by behavioral relevance. J. Neurosci. 2014, 34:1271-1279.
47. Fogassi L., Ferrari P.F., Gesierich B., Rozzi S., Chersi F., Rizzolatti G. Parietal lobe: from action organization to intention understanding. Science 2005, 308:662-667.
48. Foster D.J., Wilson M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 2006, 440:680-683.
49. Foster D.J., Morris R.G., Dayan P. A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus 2000, 10:1-16.
50. Fuhs M.C., Touretzky D.S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 2006, 26:4266-4276.
51. Gehring W.J., Knight R.T. Prefrontal-cingulate interactions in action monitoring. Nat. Neurosci. 2000, 3:516-520.
52. Guariglia C., Piccardi L., Iaria G., Nico D., Pizzamiglio L. Representational neglect and navigation in real space. Neuropsychologia 2005, 43:1138-1143.
53. Guitart-Masip M., Duzel E., Dolan R., Dayan P. Action versus valence in decision making. Trends Cogn. Sci. 2014, 18:194-202.
54. Gupta A.S., van der Meer M.A.A., Touretzky D.S., Redish A.D. Hippocampal replay is not a simple function of experience. Neuron 2010, 65:695-705.
55. Hafting T., Fyhn M., Molden S., Moser M.-B., Moser E.I.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
56. Hamilton D.A., Akers K.G., Weisend M.P., Sutherland R.J. How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector. J. Exp. Psychol. Anim. Behav. Process. 2007, 33:100-114.
57. Hardcastle K., Ganguli S., Giocomo L.M. Environmental boundaries as an error correction mechanism for grid cells. Neuron 2015, 86:827-839.
58. Hartley T., Burgess N., Lever C., Cacucci F., O'Keefe J. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 2000, 10:369-379.
59. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37:877-888.
60. Hartley T., Lever C., Burgess N., O'Keefe J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369:20120510.
61. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484:62-68.
62. Hassabis D., Maguire E.A. Deconstructing episodic memory with construction. Trends Cogn. Sci. 2007, 11:299-306.
63. Hirsh R. The hippocampus and contextual retrieval of information from memory: a theory. Behav. Biol. 1974, 12:421-444.
64. Hok V., Save E., Lenck-Santini P.P., Poucet B. Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc. Natl. Acad. Sci. USA 2005, 102:4602-4607.
65. Howard M.W., Kahana M.J. Contextual variability and serial position effects in free recall. J. Exp. Psy. Learn. Mem. Cognit. 1999, 25:923-941.
66. Hull C.L. Principles of Behavior: An Introduction to Behavior Theory 1943, Appleton-Century.
67. Hwang E.J., Hauschild M., Wilke M., Andersen R.A. Spatial and temporal eye-hand coordination relies on the parietal reach region. J. Neurosci. 2014, 34:12884-12892.
68. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J. Neurosci. 2003, 23:5945-5952.
69. Jacob P.-Y., Poucet B., Liberge M., Save E., Sargolini F. Vestibular control of entorhinal cortex activity in spatial navigation. Front. Integr. Nuerosci. 2014, 8:38.
70. Jeffery K.J., Gilbert A., Burton S., Strudwick A. Preserved performance in a hippocampal-dependent spatial task despite complete place cell remapping. Hippocampus 2003, 13:175-189.
71. Johnson A., Redish A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 2007, 27:12176-12189.
72. Káli S., Dayan P. Hippocampally-dependent consolidation in a hierarchical model of neocortex. Advances in Neural Information Processing Systems 13 2000, 24-30. NIPS 2000. T.K. Leen, T.G. Dietterich, V. Tresp (Eds.).
73. Káli S., Dayan P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat. Neurosci. 2004, 7:286-294.
74. Kamin L.J. Predictability, surprise, attention and conditioning. Punishment and aversive behavior. Punishment and Aversive Behavior 1969, 279-296. Appleton-Century-Crofts. B.A. Campbell, R.M. Church (Eds.).
75. Keramati M., Dezfouli A., Piray P. Speed/accuracy trade-off between the habitual and the goal-directed processes. PLoS Comput. Biol. 2011, 7:e1002055.
76. Killcross S., Coutureau E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 2003, 13:400-408.
77. Kim S., Dede A.J.O., Hopkins R.O., Squire L.R. Memory, scene construction, and the human hippocampus. Proc. Natl. Acad. Sci. USA 2015, 112:4767-4772.
78. Kjelstrup K.B., Solstad T., Brun V.H., Hafting T., Leutgeb S., Witter M.P., Moser E.I., Moser M.-B. Finite scale of spatial representation in the hippocampus. Science 2008, 321:140-143.
79. Knight R., Hayman R. Allocentric directional processing in the rodent and human retrosplenial cortex. Front. Hum. Neurosci. 2014, 8:135.
80. Knowlton B.J., Mangels J.A., Squire L.R. A neostriatal habit learning system in humans. Science 1996, 273:1399-1402.
81. Kraus B.J., Robinson R.J., White J.A., Eichenbaum H., Hasselmo M.E. Hippocampal "time cells": time versus path integration. Neuron 2013, 78:1090-1101.
82. Krupic J., Bauza M., Burton S., Barry C., O'Keefe J. Grid cell symmetry is shaped by environmental geometry. Nature 2015, 518:232-235.
83. Lambrey S., Doeller C., Berthoz A., Burgess N. Imagining being somewhere else: neural basis of changing perspective in space. Cereb. Cortex 2012, 22:166-174.
84. Lansink C.S., Goltstein P.M., Lankelma J.V., Joosten R.N.J.M.A., McNaughton B.L., Pennartz C.M.A. Preferential reactivation of motivationally relevant information in the ventral striatum. J. Neurosci. 2008, 28:6372-6382.
85. Lengyel M., Dayan P. Hippocampal contributions to control: the third way. Advances in Neural Information Processing Systems 20 2007, 889-896. NIPS 2007. J.C. Platt, D. Koller, Y. Singer, S.T. Roweis (Eds.).
86. Lever C., Burgess N., Cacucci F., Hartley T., O'Keefe J. What can the hippocampal representation of environmental geometry tell us about Hebbian learning?. Biol. Cybern. 2002, 87:356-372.
87. Lever C., Burton S., Jeewajee A., O'Keefe J., Burgess N. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 2009, 29:9771-9777.
88. Lin W.-J., Horner A.J., Bisby J.A., Burgess N. Medial Prefrontal Cortex: Adding Value to Imagined Scenarios. J. Cogn. Neurosci. 2015, 27:1957-1967.
89. Maaswinkel H., Whishaw I.Q. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav. Brain Res. 1999, 99:143-152.
90. Mackintosh N.J. Conditioning and Associative Learning 1983, Oxford University Press.
91. Maia T.V. Reinforcement learning, conditioning, and the brain: Successes and challenges. Cogn. Affect. Behav. Neurosci. 2009, 9:343-364.
92. Mankin E.A., Sparks F.T., Slayyeh B., Sutherland R.J., Leutgeb S., Leutgeb J.K. Neuronal code for extended time in the hippocampus. Proc. Natl. Acad. Sci. USA 2012, 109:19462-19467.
93. Manns J.R., Howard M.W., Eichenbaum H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 2007, 56:530-540.
94. Marchette S.A., Vass L.K., Ryan J., Epstein R.A. Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat. Neurosci. 2014, 17:1598-1606.
95. Markus E.J., Qin Y.L., Leonard B., Skaggs W.E., McNaughton B.L., Barnes C.A. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 1995, 15:7079-7094.
96. Marr D. A theory for cerebral neocortex. Proc. R. Soc. Lond. B Biol. Sci. 1970, 176:161-234.
97. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1971, 262:23-81.
98. Martinet L.-E., Sheynikhovich D., Benchenane K., Arleo A. Spatial learning and action planning in a prefrontal cortical network model. PLoS Comput. Biol. 2011, 7:e1002045.
99. McClelland J.L., McNaughton B.L., O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 1995, 102:419-457.
100. McNamara C.G., Tejero-Cantero Á., Trouche S., Campo-Urriza N., Dupret D. Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat. Neurosci. 2014, 17:1658-1660.
101. McNaughton B.L., Barnes C.A., O'Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 1983, 52:41-49.
102. McNaughton B.L., Mizumori S.J., Barnes C.A., Leonard B.J., Marquis M., Green E.J. Cortical representation of motion during unrestrained spatial navigation in the rat. Cereb. Cortex 1994, 4:27-39.
103. McNaughton B.L., Battaglia F.P., Jensen O., Moser E.I., Moser M.-B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 2006, 7:663-678.
104. Mizumori S.J., Williams J.D. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 1993, 13:4015-4028.
105. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
106. Moscovitch M., Nadel L., Winocur G., Gilboa A., Rosenbaum R.S. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr. Opin. Neurobiol. 2006, 16:179-190.
107. Muller R.U., Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 1987, 7:1951-1968.
108. Muller R.U., Stead M., Pach J. The hippocampus as a cognitive graph. J. Gen. Physiol. 1996, 107:663-694.
109. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., Kato A., Carr C.A., Johnston D., Wilson M.A., Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 2002, 297:211-218.
110. Nitz D.A. Tracking route progression in the posterior parietal cortex. Neuron 2006, 49:747-756.
111. O'Doherty J., Dayan P., Schultz J., Deichmann R., Friston K., Dolan R.J. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304:452-454.
112. O'Keefe J., Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature 1996, 381:425-428.
113. O'Keefe J., Conway D.H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 1978, 31:573-590.
114. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
115. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press.
116. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
117. Ólafsdóttir H.F., Barry C., Saleem A.B., Hassabis D., Spiers H.J. Hippocampal place cells construct reward related sequences through unexplored space. eLife 2015, 4:e06063.
118. Olton D.S., Walker J.A., Gage F.H., Johnson C.T. Choice behavior of rats searching for food. Learn. Motiv. 1977, 8:315-331.
119. Packard M.G., McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 1992, 106:439-446.
120. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
121. Pavlov I.P. Conditioned Reflexes 1927, Oxford Univ Press.
122. Pearce J.M., Roberts A.D., Good M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 1998, 396:75-77.
123. Pennartz C.M.A., Ito R., Verschure P.F.M.J., Battaglia F.P., Robbins T.W. The hippocampal-striatal axis in learning, prediction and goal-directed behavior. Trends Neurosci. 2011, 34:548-559.
124. Penny W.D., Zeidman P., Burgess N. Forward and backward inference in spatial cognition. PLoS Comput. Biol. 2013, 9:e1003383.
125. Petrides M. Functional organization of the human frontal cortex for mnemonic processing. Evidence from neuroimaging studies. Ann. N Y Acad. Sci. 1995, 769:85-96.
126. Pfeiffer B.E., Foster D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-79.
127. Pouget A., Sejnowski T.J. A new view of hemineglect based on the response properties of parietal neurones. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1997, 352:1449-1459.
128. Quirk G.J., Muller R.U., Kubie J.L. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 1990, 10:2008-2017.
129. Ranck J.B. Head direction cells in the deep cell layer of dorsal postsubiculum in freely moving rats. Electrical Activity of the Archicortex 1985, 217-220. Akademiai Kiado. G. Buzsáki, C.H. Vanderwolf (Eds.).
130. Rescorla R.A., Wagner A.R. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II: Current Research and Theory 1972, 64-99. Appleton-Century-Crofts. A.H. Black, W.F. Prokasy (Eds.).
131. Rowe J.B., Toni I., Josephs O., Frackowiak R.S., Passingham R.E. The prefrontal cortex: response selection or maintenance within working memory?. Science 2000, 288:1656-1660.
132. Samsonovich A., McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 1997, 17:5900-5920.
133. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.B., Moser E.I. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
134. Schacter D.L., Addis D.R. The cognitive neuroscience of constructive memory: remembering the past and imagining the future. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007, 362:773-786.
135. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
136. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. 1957. J. Neuropsychiatry Clin. Neurosci. 2000, 12:103-113.
137. Shelton A.L., Gabrieli J.D.E. Neural correlates of encoding space from route and survey perspectives. J. Neurosci. 2002, 22:2711-2717.
138. Sheynikhovich D., Chavarriaga R., Strösslin T., Arleo A., Gerstner W. Is there a geometric module for spatial orientation? Insights from a rodent navigation model. Psychol. Rev. 2009, 116:540-566.
139. Singer A.C., Carr M.F., Karlsson M.P., Frank L.M. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 2013, 77:1163-1173.
140. Skaggs W.E., Knierim J.J., Kudrimoti H., McNaughton L.B. A model of the neural basis of the rat's sense of direction. Advances in Neural Information Processing Systems 7 1994, 173-180. NIPS 1994. G. Tesauro, D.S. Touretzky, T.K. Leen (Eds.).
141. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
142. Smith K.S., Graybiel A.M. A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron 2013, 79:361-374.
143. Snyder L.H., Grieve K.L., Brotchie P., Andersen R.A. Separate body- and world-referenced representations of visual space in parietal cortex. Nature 1998, 394:887-891.
144. Solstad T., Boccara C.N., Kropff E., Moser M.-B., Moser E.I. Representation of geometric borders in the entorhinal cortex. Science 2008, 322:1865-1868.
145. Stachenfeld K., Botvinick M., Gershman S. Design principles of the hippocampal cognitive map. Advances in Neural Information Processing Systems 27 2014, 2528-2536. NIPS 2014. Z. Ghahramani, M. Welling, C. Cortes, N.D. Lawrence, K.Q. Weinberger (Eds.).
146. Stackman R.W., Taube J.S. Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J. Neurosci. 1998, 18:9020-9037.
147. Stensola H., Stensola T., Solstad T., Frøland K., Moser M.-B., Moser E.I. The entorhinal grid map is discretized. Nature 2012, 492:72-78.
148. Stensola T., Stensola H., Moser M.-B., Moser E.I. Shearing-induced asymmetry in entorhinal grid cells. Nature 2015, 518:207-212.
149. Sutton R.S., Barto A.G. Toward a modern theory of adaptive networks: expectation and prediction. Psychol. Rev. 1981, 88:135-170.
150. Taube J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 1995, 15:70-86.
151. Taube J.S., Muller R.U., Ranck J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 1990, 10:436-447.
152. Thompson L.T., Best P.J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 1990, 509:299-308.
153. Tolman E.C. Cognitive maps in rats and men. Psychol. Rev. 1948, 55:189-208.
154. Tremblay L., Schultz W. Relative reward preference in primate orbitofrontal cortex. Nature 1999, 398:704-708.
155. Tse D., Langston R.F., Kakeyama M., Bethus I., Spooner P.A., Wood E.R., Witter M.P., Morris R.G.M. Schemas and memory consolidation. Science 2007, 316:76-82.
156. Ulanovsky N., Moss C.F. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 2007, 10:224-233.
157. van der Meer M.A.A., Redish A.D. Covert Expectation-of-Reward in Rat Ventral Striatum at Decision Points. Front. Integr. Nuerosci. 2009, 3:1.
158. van der Meer M.A.A., Ito R., Lansink C.S., Pennartz C.M.A. Hippocampal Projections to the Ventral Striatum: From Spatial Memory to Motivated Behavior. Space,Time and Memory in the Hippocampal Formation 2014, 497-516. Springer Vienna. D. Derdikman, J.J. Knierim (Eds.).
159. van Strien N.M., Cappaert N.L.M., Witter M.P. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 2009, 10:272-282.
160. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 2004, 27:468-474.
161. Wallace D.G., Gorny B., Whishaw I.Q. Rats can track odors, other rats, and themselves: implications for the study of spatial behavior. Behav. Brain Res. 2002, 131:185-192.
162. Watanabe M. Reward expectancy in primate prefrontal neurons. Nature 1996, 382:629-632.
163. Whitlock J.R., Pfuhl G., Dagslott N., Moser M.-B., Moser E.I. Functional split between parietal and entorhinal cortices in the rat. Neuron 2012, 73:789-802.
164. Wikenheiser A.M., Redish A.D. The balance of forward and backward hippocampal sequences shifts across behavioral states. Hippocampus 2013, 23:22-29.
165. Wilber A.A., Clark B.J., Forster T.C., Tatsuno M., McNaughton B.L. Interaction of egocentric and world-centered reference frames in the rat posterior parietal cortex. J. Neurosci. 2014, 34:5431-5446.
166. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
167. Wolbers T., Büchel C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J. Neurosci. 2005, 25:3333-3340.
168. Wood E.R., Dudchenko P.A., Robitsek R.J., Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000, 27:623-633.
169. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 2006, 7:464-476.
170. Yoon K., Buice M.A., Barry C., Hayman R., Burgess N., Fiete I.R. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 2013, 16:1077-1084.
171. Zhang K. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 1996, 16:2112-2126.
172. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 2013, 16:264-266.