The role of the hippocampus in navigation is memory

Journal of Neurophysiology

Volumn 117, Issue 4, 2017, Pages 1785-1796

  Eichenbaum, Howard ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

Cognitive map; Hippocampus; Memory; Navigation

Indexed keywords

ASSOCIATION; BRAIN FUNCTION; BRAIN MAPPING; COGNITION; COGNITIVE MAP; EVOLUTION; HIPPOCAMPUS; HUMAN; KNOWLEDGE; LEARNING; MEMORY; NONHUMAN; PERSONAL EXPERIENCE; PRIORITY JOURNAL; REVIEW; SPATIAL ORIENTATION; ANIMAL; DEPTH PERCEPTION; PHYSIOLOGY;

ANIMALS; COGNITION; HIPPOCAMPUS; HUMANS; MEMORY; SPACE PERCEPTION; SPATIAL NAVIGATION;

EID: 85017303048     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00005.2017     Document Type: Review

References (117)

1. Ainge JA, Tamosiunaite M, Woergoetter F, Dudchenko PA. Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. J Neurosci 27: 9769-9779, 2007b. doi:10.1523/JNEUROSCI.2011-07.2007.
2. Ainge JA, van der Meer MA, Langston RF, Wood ER. Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 17: 988-1002, 2007a. doi:10.1002/hipo.20301.
3. Alyan S, McNaughton BL. Hippocampectomized rats are capable of homing by path integration. Behav Neurosci 113: 19-31, 1999. doi:10.1037/0735-7044.113.1.19.
4. Aronov D, Nevers R, Tank DW. Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit. Nature 543: 719-722, 2017. doi:10.1038/ nature21692.
5. Bahar AS, Shapiro ML. Remembering to learn: independent place and journey coding mechanisms contribute to memory transfer. J Neurosci 32: 2191-2203, 2012. doi:10.1523/JNEUROSCI.3998-11.2012.
6. Benhamou S. Path integration by swimming rats. Anim Behav 54: 321-327, 1997. doi:10.1006/anbe.1996.0464.
7. 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. doi:10.1523/JNEUROSCI. 2901-04.2005.
8. Brown TI, Carr VA, LaRocque KF, Favila SE, Gordon AM, Bowles B, Bailenson JN, Wagner AD. Prospective representation of navigational goals in the human hippocampus. Science 352: 1323-1326, 2016. doi:10. 1126/science.aaf0784.
9. Bunsey M, Eichenbaum H. Conservation of hippocampal memory function in rats and humans. Nature 379: 255-257, 1996. doi:10.1038/379255a0.
10. Buzsáki G, Moser EI. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16: 130-138, 2013. doi:10.1038/nn. 3304.
11. Chen G, Manson D, Cacucci F, Wills TJ. Absence of visual input results in the disruption of grid cell firing in the mouse. Curr Biol 26: 2335-2342, 2016. doi:10.1016/j.cub.2016.06.043.
12. Cheng K. A purely geometric module in the rat’s spatial representation. Cognition 23: 149-178, 1986. doi:10.1016/0010-0277(86)90041-7.
13. Chersi F, Burgess N. The cognitive architecture of spatial navigation: hippocampal and striatal contributions. Neuron 88: 64-77, 2015. doi:10.1016/ j.neuron.2015.09.021.
14. Colgin LL, Moser EI, Moser MB. Understanding memory through hippocampal remapping. Trends Neurosci 31: 469-477, 2008. doi:10.1016/j. tins.2008.06.008.
15. Collett TS, Cartwright BA, Smith BA. Landmark learning and visuo-spatial memories in gerbils. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 158: 835-851, 1986. doi:10.1007/BF01324825.
16. Constantinescu AO, O’Reilly JX, Behrens TE. Organizing conceptual knowledge in humans with a gridlike code. Science 352: 1464-1468, 2016. doi:10.1126/science.aaf0941.
17. Dede AJ, Frascino JC, Wixted JT, Squire LR. Learning and remembering real-world events after medial temporal lobe damage. Proc Natl Acad Sci USA 113: 13480-13485, 2016. doi:10.1073/pnas.1617025113.
18. Derdikman D, Moser EI. A manifold of spatial maps in the brain. Trends Cogn Sci 14: 561-569, 2010. doi:10.1016/j.tics.2010.09.004.
19. Devito LM, Kanter BR, Eichenbaum H. The hippocampus contributes to memory expression during transitive inference in mice. Hippocampus 20: 208-217, 2010.
20. Dudchenko PA. Why people get lost: The Psychology and Neuroscience of Spatial Cognition. New York: Oxford University Press, 2010.
21. Dupret D, O’Neill J, Pleydell-Bouverie B, Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci 13: 995-1002, 2010. doi:10.1038/nn.2599.
22. Dusek JA, Eichenbaum H. The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci USA 94: 7109-7114, 1997. doi:10. 1073/pnas.94.13.7109.
23. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109-120, 2004. doi:10.1016/ j.neuron.2004.08.028.
24. Eichenbaum H. Time cells in the hippocampus: a new dimension for mapping memories. Nat Rev Neurosci 15: 732-744, 2014. doi:10.1038/nrn3827.
25. Eichenbaum H. Memory: organization and control. Annu Rev Psychol 68: 19-45, 2017. doi:10.1146/annurev-psych-010416-044131.
26. Eichenbaum H, Cohen NJ. Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83: 764-770, 2014. doi:10.1016/j.neuron.2014.07.032.
27. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23: 209-226, 1999. doi:10.1016/S0896-6273(00)80773-4.
28. Eichenbaum H, Stewart C, Morris RGM. Hippocampal representation in place learning. J Neurosci 10: 3531-3542, 1990.
29. Eichenbaum H, Yonelinas AP, Ranganath C. The medial temporal lobe and recognition memory. Annu Rev Neurosci 30: 123-152, 2007. doi:10.1146/annurev.neuro.30.051606.094328.
30. Ferbinteanu J, Shapiro ML. Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227-1239, 2003. doi:10.1016/S0896-6273 (03)00752-9.
31. Fortin NJ, Agster KL, Eichenbaum HB. Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5: 458-462, 2002. doi:10. 1038/nn834.
32. Fouquet C, Babayan BM, Watilliaux A, Bontempi B, Tobin C, Rondi-Reig L. Complementary roles of the hippocampus and the dorsomedial striatum during spatial and sequence-based navigation behavior. PLoS One 8: e67232, 2013. doi:10.1371/journal.pone.0067232.
33. Frank LM, Brown EN, Wilson M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27: 169-178, 2000. doi:10.1016/S0896-6273(00)00018-0.
34. Franz MO, Mallot HA. Biomimetic robot navigation. Rob Auton Syst 30: 133-153, 2000. doi:10.1016/S0921-8890(99)00069-X.
35. Gallistel CR. The Organization of Learning. Cambridge, MA: Bradford Books/MIT Press, 1990.
36. Gallistel CR. Navigation: whence our sense of direction? Curr Biol 27: R108-R110, 2017. doi:10.1016/j.cub.2016.11.044.
37. Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat Rev Neurosci 16: 94-108, 2015. doi:10.1038/nrn3888.
38. Geva-Sagiv M, Romani S, Las L, Ulanovsky N. Hippocampal global remapping for different sensory modalities in flying bats. Nat Neurosci 19: 952-958, 2016. doi:10.1038/nn.4310.
39. Gothard KM, Skaggs WE, McNaughton BL. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16: 8027-8040, 1996.
40. 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. doi:10.1523/ JNEUROSCI.4083-06.2007.
41. Hallock HL, Griffin AL. Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand. Hippocampus 23: 169-186, 2013. doi:10.1002/hipo.22079.
42. Hartley T, Burgess N. Complementary memory systems: competition, cooperation and compensation. Trends Neurosci 28: 169-170, 2005. doi:10. 1016/j.tins.2005.02.004.
43. 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 369: 20120510, 2013. doi:10.1098/rstb.2012.0510.
44. Hartley T, Maguire EA, Spiers HJ, Burgess N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37: 877-888, 2003. doi:10.1016/S0896-6273(03)00095-3.
45. Huth JE. The Lost Art of Finding Our Way. Cambridge, MA: Harvard University Press, 2013. doi:10.4159/harvard.9780674074811
46. 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.
47. Johnson A, Redish AD. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27: 12176-12189, 2007. doi:10.1523/JNEUROSCI.3761-07.2007.
48. Keinath AT, Julian JB, Epstein RA, Muzzio IA. Environmental geometry aligns the hippocampal map during spatial reorientation. Curr Biol 27: 309-317, 2017. doi:10.1016/j.cub.2016.11.046.
49. Kelemen E, Fenton AA. Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol 8: e1000403, 2010. doi:10.1371/journal.pbio.1000403.
50. Kesner RP, Gilbert PE, Barua LA. The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav Neurosci 116: 286-290, 2002. doi:10.1037/0735-7044.116.2.286.
51. Kim S, Sapiurka M, Clark RE, Squire LR. Contrasting effects on path integration after hippocampal damage in humans and rats. Proc Natl Acad Sci USA 110: 4732-4737, 2013. doi:10.1073/pnas.1300869110.
52. Kraus BJ, Brandon MP, Robinson RJ, II, Connerney MA, Hasselmo ME, Eichenbaum H. During running in place, grid cells integrate elapsed time and distance run. Neuron 88: 578-589, 2015. doi:10.1016/j.neuron.2015. 09.031.
53. Kraus BJ, Robinson RJ II, White JA, Eichenbaum H, Hasselmo ME. Hippocampal “time cells”: time versus path integration. Neuron 78: 1090-1101, 2013. doi:10.1016/j.neuron.2013.04.015.
54. Kropff E, Carmichael JE, Moser MB, Moser EI. Speed cells in the medial entorhinal cortex. Nature 523: 419-424, 2015. doi:10.1038/nature14622.
55. Lazareva OF, Kandray K, Acerbo MJ. Hippocampal lesion and transitive inference: dissociation of inference-based and reinforcement-based strategies in pigeons. Hippocampus 25: 219-226, 2015. doi:10.1002/hipo.22366.
56. 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, 2001. doi:10.1046/j.0953-816x.2001.01481.x.
57. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-623, 2005. doi:10.1126/science. 1114037.
58. Levitt TS, Lawton DT. Qualitative navigation for mobile robots. Artif Intell 44: 305-360, 1990. doi:10.1016/0004-3702(90)90027-W.
59. Lipton PA, Eichenbaum H. Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural Plast 2008: 258467, 2008. doi:10.1155/2008/258467.
60. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J. Knowing where and getting there: a human navigation network. Science 280: 921-924, 1998. doi:10.1126/science.280.5365.921.
61. Maguire EA, Frackowiak RS, Frith CD. Recalling routes around London: activation of the right hippocampus in taxi drivers. J Neurosci 17: 7103-7110, 1997.
62. Markus EJ, Qin Y-L, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079-7094, 1995.
63. Maza FJ, Sztarker J, Shkedy A, Peszano VN, Locatelli FF, Delorenzi A. Context-dependent memory traces in the crab’s mushroom bodies: functional support for a common origin of high-order memory centers. Proc Natl Acad Sci USA 113: E7957-E7965, 2016. doi:10.1073/pnas.1612418113.
64. 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. doi:10.1016/S0163-1047(05)80009-3.
65. McKenzie S, Frank AJ, Kinsky NR, Porter B, Rivière PD, Eichenbaum H. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83: 202-215, 2014. doi:10.1016/j.neuron.2014.05.019.
66. McKenzie S, Robinson NTM, Herrera L, Churchill JC, Eichenbaum H. Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J Neurosci 33: 10243-10256, 2013. doi:10.1523/JNEUROSCI.0879-13.2013.
67. McNamara TP, Shelton AL. Cognitive maps and the hippocampus. Trends Cogn Sci 7: 333-335, 2003. doi:10.1016/S1364-6613(03)00167-0.
68. McNaughton BL, Barnes CA, O’Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freelymoving rats. Exp Brain Res 52: 41-49, 1983. doi:10.1007/BF00237147.
69. 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. doi:10.1038/nrn1932.
70. Milivojevic B, Doeller CF. Mnemonic networks in the hippocampal formation: from spatial maps to temporal and conceptual codes. J Exp Psychol Gen 142: 1231-1241, 2013. doi:10.1037/a0033746.
71. Milivojevic B, Vicente-Grabovetsky A, Doeller CF. Insight reconfigures hippocampal-prefrontal memories. Curr Biol 25: 821-830, 2015. doi:10. 1016/j.cub.2015.01.033.
72. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT. Putting fear in its place: remapping of hippocampal place cells during fear conditioning. J Neurosci 24: 7015-7023, 2004. doi:10.1523/JNEUROSCI.5492-03.2004.
73. Morris RG. Spatial localization does not require the presence of local cues. Learn Motiv 12: 239-260, 1981. doi:10.1016/0023-9690(81)90020-5.
74. Morris RG, Garrud P, Rawlins JN, O’Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683, 1982. doi:10.1038/ 297681a0.
75. Moser EI, Kropff E, Moser MB. Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31: 69-89, 2008. doi:10.1146/ annurev.neuro.31.061307.090723.
76. Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, Stead M, Abbott LF, Kandel ER. Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol 7: e1000140, 2009. doi:10.1371/journal.pbio.1000140.
77. Naya Y, Suzuki WA. Integrating what and when across the primate medial temporal lobe. Science 333: 773-776, 2011. doi:10.1126/science.1206773.
78. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: 171-175, 1971. doi:10.1016/0006-8993(71)90358-1.
79. O’Keefe J, Nadel L. The Hippocampus as a Cognitive Map. New York: Oxford University Press, 1978.
80. 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. doi:10.1006/nlme.1996.0007.
81. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 321: 1322-1327, 2008. doi:10.1126/science.1159775.
82. Paz R, Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I. A neural substrate in the human hippocampus for linking successive events. Proc Natl Acad Sci USA 107: 6046-6051, 2010. doi:10.1073/pnas. 0910834107.
83. Pecchia T, Vallortigara G. View-based strategy for reorientation by geometry. J Exp Biol 213: 2987-2996, 2010. doi:10.1242/jeb.043315.
84. Pfeiffer BE, Foster DJ. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497: 74-79, 2013. doi:10.1038/nature12112.
85. Poucet B. Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol Rev 100: 163-182, 1993. doi:10.1037/ 0033-295X.100.2.163.
86. Preston AR, Shrager Y, Dudukovic NM, Gabrieli JD. Hippocampal contribution to the novel use of relational information in declarative memory. Hippocampus 14: 148-152, 2004. doi:10.1002/hipo.20009.
87. Ranck JB Jr. Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10: 599, 1984.
88. Robitsek RJ, White JA, Eichenbaum H. Place cell activation predicts subsequent memory. Behav Brain Res 254: 65-72, 2013. doi:10.1016/j.bbr. 2012.12.034.
89. Rosenbaum RS, Priselac S, Köhler S, Black SE, Gao F, Nadel L, Moscovitch M. Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions. Nat Neurosci 3: 1044-1048, 2000. doi:10. 1038/79867.
90. Sarel A, Finkelstein A, Las L, Ulanovsky N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355: 176-180, 2017. doi:10.1126/science.aak9589.
91. Schiller D, Eichenbaum H, Buffalo EA, Davachi L, Foster DJ, Leutgeb S, Ranganath C. Memory and space: towards an understanding of the cognitive map. J Neurosci 35: 13904-13911, 2015. doi:10.1523/JNEUROSCI. 2618-15.2015.
92. Shrager Y, Bayley PJ, Bontempi B, Hopkins RO, Squire LR. Spatial memory and the human hippocampus. Proc Natl Acad Sci USA 104: 2961-2966, 2007. doi:10.1073/pnas.0611233104.
93. Shrager Y, Kirwan CB, Squire LR. Neural basis of the cognitive map: path integration does not require hippocampus or entorhinal cortex. Proc Natl Acad Sci USA 105: 12034-12038, 2008. doi:10.1073/pnas.0805414105.
94. Smith DM, Mizumori SJ. Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J Neurosci 26: 3154-3163, 2006. doi:10.1523/JNEUROSCI. 3234-05.2006.
95. Spiers HJ, Burgess N, Hartley T, Vargha-Khadem F, O’Keefe J. Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching. Hippocampus 11: 715-725, 2001. doi:10.1002/ hipo.1087.
96. Spiers HJ, Maguire EA. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31: 1826-1840, 2006. doi:10. 1016/j.neuroimage.2006.01.037.
97. Spiers HJ, Maguire EA. The dynamic nature of cognition during wayfinding. J Environ Psychol 28: 232-249, 2008. doi:10.1016/j.jenvp.2008.02.006.
98. Squire LR, Stark CEL, Clark RE. The medial temporal lobe. Annu Rev Neurosci 27: 279-306, 2004. doi:10.1146/annurev.neuro.27.070203. 144130.
99. Suthana NA, Ekstrom AD, Moshirvaziri S, Knowlton B, Bookheimer SY. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J Neurosci 29: 10512-10519, 2009. doi:10.1523/JNEUROSCI. 0621-09.2009.
100. Taube JS, Muller RU, Ranck JB Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10: 420-435, 1990.
101. Tavares RM, Mendelsohn A, Grossman Y, Williams CH, Shapiro M, Trope Y, Schiller D. A Map for Social Navigation in the Human Brain. Neuron 87: 231-243, 2015. doi:10.1016/j.neuron.2015.06.011.
102. Teng E, Squire LR. Memory for places learned long ago is intact after hippocampal damage. Nature 400: 675-677, 1999. doi:10.1038/23276.
103. Tolman EC. Cognitive maps in rats and men. Psychol Rev 55: 189-208, 1948. doi:10.1037/h0061626.
104. Trullier O, Wiener SI, Berthoz A, Meyer JA. Biologically based artificial navigation systems: review and prospects. Prog Neurobiol 51: 483-544, 1997. doi:10.1016/S0301-0082(96)00060-3.
105. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RG. Schemas and memory consolidation. Science 316: 76-82, 2007. doi:10.1126/science.1135935.
106. Urgolites ZJ, Kim S, Hopkins RO, Squire LR. Map reading, navigating from maps, and the medial temporal lobe. Proc Natl Acad Sci USA 113: 14289-14293, 2016. doi:10.1073/pnas.1617786113.
107. Voermans NC, Petersson KM, Daudey L, Weber B, Van Spaendonck KP, Kremer HP, Fernández G. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 43: 427-435, 2004. doi:10.1016/j.neuron.2004.07.009.
108. Wang ME, Wann EG, Yuan RK, Ramos Álvarez MM, Stead SM, Muzzio IA. Long-term stabilization of place cell remapping produced by a fearful experience. J Neurosci 32: 15802-15814, 2012. doi:10.1523/JNEUROSCI. 0480-12.2012.
109. Wang ME, Yuan RK, Keinath AT, Ramos Álvarez MM, Muzzio IA. Extinction of learned fear induces hippocampal place cell remapping. J Neurosci 35: 9122-9136, 2015. doi:10.1523/JNEUROSCI.4477-14.2015.
110. Whishaw IQ, Hines DJ, Wallace DG. Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests. Behav Brain Res 127: 49-69, 2001. doi:10.1016/S0166-4328(01)00359-X.
111. Whishaw IQ, Maaswinkel H. Rats with fimbria-fornix lesions are impaired in path integration: a role for the hippocampus in “sense of direction”. J Neurosci 18: 3050-3058, 1998.
112. Winocur G, Moscovitch M, Fogel S, Rosenbaum RS, Sekeres M. Preserved spatial memory after hippocampal lesions: effects of extensive experience in a complex environment. Nat Neurosci 8: 273-275, 2005. doi:10.1038/ nn1401.
113. Wolbers T, Büchel C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J Neurosci 25: 3333-3340, 2005. doi:10.1523/JNEUROSCI.4705-04.2005.
114. Wolbers T, Hegarty M. What determines our navigational abilities? Trends Cogn Sci 14: 138-146, 2010. doi:10.1016/j.tics.2010.01.001.
115. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623-633, 2000. doi:10.1016/ S0896-6273(00)00071-4.
116. Zalesak M, Heckers S. The role of the hippocampus in transitive inference. Psychiatry Res 172: 24-30, 2009. doi:10.1016/j.pscychresns.2008. 09.008.
117. Zeithamova D, Dominick AL, Preston AR. Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron 75: 168-179, 2012. doi:10.1016/j.neuron.2012.05.010.