Cues, context, and long-term memory: The role of the retrosplenial cortex in spatial cognition

Frontiers in Human Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Miller, Adam P ^a   Vedder, Lindsey C ^a   Law, Matthew L ^a   Smith, David M ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Allocentric; Consolidation; Context; Hippocampus; Learning; Long term memory; Navigation; Retrosplenial cortex

Indexed keywords

AMNESIA; ANTERIOR THALAMUS; ASSOCIATION; BIOLOGICAL MODEL; BRAIN DAMAGE; COGNITION; CONCEPTUAL FRAMEWORK; DISEASE SEVERITY; EPISODIC MEMORY; FUNCTIONAL ANATOMY; FUNCTIONAL ASSESSMENT; HIPPOCAMPUS; HUMAN; LEARNING; LIMBIC SYSTEM; LONG TERM MEMORY; MEMORY CONSOLIDATION; MENTAL DEVELOPMENT; MENTAL TEST; NEURONAVIGATION; NONHUMAN; POSTERIOR PARIETAL CORTEX; RETROSPLENIAL CORTEX; REVIEW; SPATIAL COGNITION; SPATIAL MEMORY; THALAMUS;

EID: 84905573617     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00586     Document Type: Review

References (160)

1. Aggleton, J. P. (2008). EPS Mid-Career Award 2006. Understanding anterograde amnesia: disconnections and hidden lesions. Q. J. Exp. Psychol. (Hove) 61, 1441-1471. doi: 10.1080/17470210802215335
2. Aguirre, G. K., and D'Esposito, M. (1999). Topographical disorientation: a syn-thesis and taxonomy. Brain 122(Pt. 9), 1613-1628. doi: 10.1093/brain/122.9.1613
3. Aguirre, G. K., Detre, J. A., Alsop, D. C., and D'Esposito, M. (1996). The parahip-pocampus subserves topographical learning in man. Cereb. Cortex 6, 823-829. doi: 10.1093/cercor/6.6.823
4. Albasser, M. M., Poirier, G. L., Warburton, E. C., and Aggleton, J. P. (2007). Hippocampal lesions halve immediate-early gene protein counts in retrosplenial cortex: distal dysfunctions in a spatial memory system. Eur. J. Neurosci. 26, 1254-1266. doi: 10.1111/j.1460-9568.2007.05753.x
5. Anderson, M. I., and Jeffery, K. J. (2003). Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827-8835.
6. Auger, S. D., and Maguire, E. A. (2013). Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators. Cortex 49, 2904-2913. doi: 10.1016/j.cortex.2013.08.002
7. Auger, S. D., Mullally, S. L., and Maguire, E. A. (2012). Retrosplenial cortex codes for permanent landmarks. PLoS One 7:e43620. doi: 10.1371/journal.pone.0043620
8. Balsam, P., and Tomie, A. (1985). Context and Learning. Hillsdale, NJ: Psychology Press.
9. Bar, M. (2004). Visual objects in context. Nat. Rev. Neurosci. 5, 617-629. doi: 10. 1038/nrn1476
10. Bar, M., Aminoff, E., Mason, M., and Fenske, M. (2007). The units of thought. Hippocampus 17, 420-428. doi: 10.1002/hipo.20287
11. Bar, M., and Aminoff, E. (2003). Cortical analysis of visual context. Neuron 38, 347-358. doi: 10.1016/s0896-6273(03)00167-3
12. Biederman, I., Mezzanotte, R. J., and Rabinowitz, J. C. (1982). Scene perception: detecting and judging objects undergoing relational violations. Cogn. Psychol. 14, 143-177. doi: 10.1016/0010-0285(82)90007-x
13. Bilalić, M., Turella, L., Campitelli, G., Erb, M., and Grodd, W. (2012). Expertise modulates the neural basis of context dependent recognition of objects and their relations. Hum. Brain Mapp. 33, 2728-2740. doi: 10.1002/hbm.21396
14. Bisiach, E., Brouchon, M., Poncet, M., and Rusconi, M. L. (1993). Unilateral neglect in route description. Neuropsychologia 31, 1255-1262. doi: 10.1016/0028-3932(93)90072-8
15. Bisiach, E., and Luzzatti, C. (1978). Unilateral neglect of representational space. Cortex 14, 129-133. doi: 10.1016/s0010-9452(78)80016-1
16. Borst, J. G., Leung, L. W., and MacFabe, D. F. (1987). Electrical activity of the cingulate cortex. II. Cholinergic modulation. Brain Res. 407, 81-93. doi: 10.1016/0006-8993(87)91221-2
17. Bowers, D., Verfaellie, M., Valenstein, E., and Heilman, K. M. (1988). Impaired acquisition of temporal information in retrosplenial amnesia. Brain Cogn. 8, 47-66. doi: 10.1016/0278-2626(88)90038-3
18. Brandon, M. P., Bogaard, A. R., Schultheiss, N. W., and Hasselmo, M. E. (2013). Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat. Neurosci. 16, 739-748. doi: 10.1038/nn.3383
19. Bucci, D. J., Saddoris, M. P., and Burwell, R. D. (2002). Contextual fear discrim-ination is impaired by damage to the postrhinal or perirhinal cortex. Behav. Neurosci. 116, 479-488. doi: 10.1037/0735-7044.116.3.479
20. Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function and relevance to disease. Ann. N Y Acad. Sci. 1124, 1-38. doi: 10.1196/annals.1440.011
21. Buckner, R. L., and Carroll, D. C. (2007). Self-projection and the brain. Trends Cogn. Sci. 11, 49-57. doi: 10.1016/j.tics.2006.11.004
22. Buckner, R. L., Snyder, A. Z., Shannon, B. J., Larossa, G., Sachs, R., Fotenos, A. F., et al. (2005). Molecular, structural and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid and memory. J. Neurosci. 25, 7709-7717. doi: 10.1523/jneurosci.2177-05.2005
23. Burwell, R. D., and Amaral, D. G. (1998). Cortical afferents of the perirhinal, postrhinal and entorhinal cortices of the rat. J. Comp. Neurol. 398, 179-205.doi: 10.1002/(sici)1096-9861(19980824)398:2;179::aid-cne3>3.0.co;2-y
24. Bussey, T. J., Muir, J. L., Everitt, B. J., and Robbins, T. W. (1996). Dissociable effects of anterior and posterior cingulate cortex lesions on the acquisition of a conditional visual discrimination: facilitation of early learning vs. impairment of late learning. Behav. Brain Res. 82, 45-56. doi: 10.1016/s016-4328(97)81107-2
25. Bussey, T. J., and Saksida, L. M. (2007). Memory, perception and the ventral visual-perirhinal-hippocampal stream: thinking outside of the boxes. Hippocampus 17, 898-908. doi: 10.1002/hipo.20320
26. Butterly, D. A., Petroccione, M. A., and Smith, D. M. (2012). Hippocampal context processing is critical for interference free recall of odor memories in rats. Hippocampus 22, 906-913. doi: 10.1002/hipo.20953
27. Buzsáki, G. (2005). Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827-840. doi: 10.1002/hipo.20113
28. Calton, J. L., and Taube, J. S. (2009). Where am I and how will I get there from here? A role for posterior parietal cortex in the integration of spatial information and route planning. Neurobiol. Learn. Mem. 91, 186-196. doi: 10.1016/j.nlm.2008.09.015
29. Calton, J. L., Stackman, R. W., Goodridge, J. P., Archey, W. B., Dudchenko, P. A., and Taube, J. S. (2003). Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23, 9719-9731.
30. Carr, M. F., Jadhav, S. P., and Frank, L. M. (2011). Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147-153. doi: 10.1038/nn.2732
31. Chadwick, M. J., Mullally, S. L., and Maguire, E. A. (2013). The hippocampus extrapolates beyond the view in scenes: an fMRI study of boundary extension. Cortex 49, 2067-2079. doi: 10.1016/j.cortex.2012.11.010
32. Chase, W. G., and Simon, H. A. (1973). Perception in chess. Cogn. Psychol. 4, 55-81. doi: 10.1016/0010-0285(73)90004-2
33. Chen, L. L., Lin, L. H., Barnes, C. A., and McNaughton, B. L. (1994a). Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp. Brain Res. 101, 24-34. doi: 10.1007/bf00243213
34. Chen, L. L., Lin, L. H., Green, E. J., Barnes, C. A., and McNaughton, B. L. (1994b). Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101, 8-23. doi: 10.1007/bf00243212
35. Cho, J., and Sharp, P. E. (2001). Head direction, place and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115, 3-25.doi: 10.1037//0735-7044.115.1.3
36. Clark, B. J., Bassett, J. P., Wang, S. S., and Taube, J. S. (2010). Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J. Neurosci. 30, 5289-5302. doi: 10.1523/JNEUROSCI.3380-09.2010
37. Cooper, B. G., and Mizumori, S. J. (2001). Temporary inactivation of the ret-rosplenial cortex causes a transient reorganization of spatial coding in the hippocampus. J. Neurosci. 21, 3986-4001.
38. Corcoran, K. A., Donnan, M. D., Tronson, N. C., Guzman, Y. F., Gao, C., Jovasevic, V., et al. (2011). NMDA receptors in retrosplenial cortex are necessary for retrieval of recent and remote context fear memory. J. Neurosci. 31, 11655-11659. doi: 10.1523/JNEUROSCI.2107-11.2011
39. Danker, J. F., and Anderson, J. R. (2010). The ghosts of brain states past: remem-bering reactivates the brain regions engaged during encoding. Psychol. Bull. 136, 87-102. doi: 10.1037/a0017937
40. Day, M., Langston, R., and Morris, R. G. (2003). Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205-209. doi: 10.1038/nature01769
41. Debiec, J., LeDoux, J. E., and Nader, K. (2002). Cellular and systems reconsolidation in the hippocampus. Neuron 36, 527-538. doi: 10.1016/s0896-6273(02)01001-2
42. Dilks, D. D., Julian, J. B., Kubilius, J., Spelke, E. S., and Kanwisher, N. (2011). Mirror-image sensitivity and invariance in object and scene processing path-ways. J. Neurosci. 31, 11305-11312. doi: 10.1523/JNEUROSCI.1935-11.2011
43. Dudai, Y. (2012). The restless engram: consolidations never end. Annu. Rev. Neurosci. 35, 227-247. doi: 10.1146/annurev-neuro-062111-150500
44. Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., and Tanila, H. (1999). The hippocampus, memory and place cells: is it spatial memory or a memory space? Neuron 23, 209-226. doi: 10.1016/S0896-6273(00)80773-4
45. Epstein, R., and Kanwisher, N. (1998). A cortical representation of the local visual environment. Nature 392, 598-601. doi: 10.1038/33402
46. Epstein, R. A., Parker, W. E., and Feiler, A. M. (2007). Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J. Neurosci. 27, 6141-6149. doi: 10.1523/jneurosci.0799-07.2007
47. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U S A 102, 9673-9678. doi: 10.1073/pnas.0504136102
48. Frank, L. M., Stanley, G. B., and Brown, E. N. (2004). Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 24, 7681-7689. doi: 10.1523/jneurosci.1958-04.2004
49. Frankland, P. W., and Bontempi, B. (2005). The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119-130. doi: 10.1038/nrn1607
50. Freeman, J. H. Jr., and Gabriel, M. (1999). Changes of cingulothalamic topographic excitation patterns and avoidance response incubation over time following initial discriminative conditioning in rabbits. Neurobiol. Learn. Mem. 72, 259-272. doi: 0.1006/nlme.1998.3896
51. Freeman, J. H. Jr., Weible, A., Rossi, J., and Gabriel, M. (1997). Lesions of the entorhinal cortex disrupt behavioral and neuronal responses to context changeduring extinction of discriminative avoidance behavior. Exp. Brain Res. 115, 445-457. doi: 10.1007/pl00005714
52. Gabriel, M. (1993). Discriminative avoidance learning: a model system, in Neuro-biology of Cingulate Cortex and Limbic Thalamus, eds B. A. Vogt and M. Gabriel (Boston: Birkhäuser), 478-523.
53. Gainotti, G., Almonti, S., Di Betta, A. M., and Silveri, M. C. (1998). Retrograde amnesia in a patient with retrosplenial tumour. Neurocase 4, 519-526.doi: 10. 1093/neucas/4.6.519
54. Garden, D. L., Massey, P. V., Caruana, D. A., Johnson, B., Warburton, E. C., Aggleton, J. P., et al. (2009). Anterior thalamic lesions stop synaptic plasticity in retrosplenial cortex slices: expanding the pathology of diencephalic amnesia. Brain 132, 1847-1857. doi: 10.1093/brain/awp090
55. Good, M., and Honey, R. C. (1991). Conditioning and contextual retrieval in hippocampal rats. Behav. Neurosci. 105, 499-509.doi: 10.1037//0735-7044.105.4.499
56. Goodale, M. A., and Milner, A. D. (1992). Separate visual pathways for perception and action. Trends Neurosci. 15, 20-25. doi: 10.1016/0166-2236(92)90344-8
57. Grön, G., Wunderlich, A. P., Spitzer, M., Tomczak, R., and Riepe, M. W. (2000). Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat. Neurosci. 3, 404-408.doi: 10.1038/73980
58. Gusev, P. A., and Gubin, A. N. (2010). Arc/Arg3.1 mRNA global expression patterns elicited by memory recall in cerebral cortex differ for remote versus recent spatial memories. Front. Integr. Neurosci. 4:15. doi: 10.3389/fnint.2010.00015
59. Haijima, A., and Ichitani, Y. (2012). Dissociable anterograde amnesic effects of retrosplenial cortex and hippocampal lesions on spontaneous object recognition memory in rats. Hippocampus 22, 1868-1875. doi: 10.1002/hipo.22021
60. Harker, K. T., and Whishaw, I. Q. (2004). Impaired place navigation in place and matching-to-place swimming pool tasks follows both retrosplenial cortex lesions and cingulum bundle lesions in rats. Hippocampus 14, 224-231.doi: 10.1002/hipo.10159
61. Hart, M., Poremba, A., and Gabriel, M. (1997). The nomadic engram: overtraining eliminates the impairment of discriminative avoidance behavior produced by limbic thalamic lesions. Behav. Brain Res. 82, 169-177. doi: 10.1016/s0166-4328(97)80986-2
62. Hassabis, D., and Maguire, E. A. (2007). Deconstructing episodic memory with construction. Trends Cogn. Sci. 11, 299-306. doi: 10.1016/j.tics.2007.05.001
63. Iaria, G., Chen, J. K., Guariglia, C., Ptito, A., and Petrides, M. (2007). Retrosplenial and hippocampal brain regions in human navigation: complementary func-tional contributions to the formation and use of cognitive maps. Eur. J. Neurosci. 25, 890-899. doi: 10.1111/j.1460-9568.2007.05371.x
64. Ino, T., Doi, T., Hirose, S., Kimura, T., Ito, J., and Fukuyama, H. (2007). Directional disorientation following left retrosplenial hemorrhage: a case report with fMRI studies. Cortex 43, 248-254. doi: 10.1016/s0010-9452(08)70479-9
65. Insausti, R., Amaral, D. G., and Cowan, W. M. (1987). The entorhinal cortex of the monkey: II. Cortical afferents. J. Comp. Neurol. 264, 356-395. doi: 10.1002/cne. 902640306
66. Intraub, H., Gottesman, C. V., Willey, E. V., and Zuk, I. J. (1996). Boundary extension for briefly glimpsed photographs: do common perceptual processes result in unexpected memory distortions? J. Mem. Lang. 35, 118-134. doi: 10. 1006/jmla.1996.0007
67. Izquierdo, I., and Medina, J. H. (1997). Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68, 285-316. doi: 10.1006/nlme.1997. 3799
68. Jackson, S. R., Newport, R., Husain, M., Fowlie, J. E., O'Donoghue, M., and Bajaj, N. (2009). There may be more to reaching than meets the eye: re-thinking optic ataxia. Neuropsychologia 47, 1397-1408. doi: 10.1016/j.neuropsychologia.2009. 01.035
69. Jenkins, T. A., Vann, S. D., Amin, E., and Aggleton, J. P. (2004). Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosple-nial cortex: evidence of covert pathology in rats? Eur. J. Neurosci. 19, 3291-3304. doi: 10.1111/j.0953-816x.2004.03421.x
70. Jones, M. W., and Wilson, M. A. (2005). Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3:e402.doi: 10. 1371/journal.pbio.0030402
71. Kang, E., and Gabriel, M. (1998). Hippocampal modulation of cingulo-thalamic neuronal activity and discriminative avoidance learning in rabbits. Hippocampus 8, 491-510. doi: 10.1002/(sici)1098-1063(1998)8:5;491::aid-hipo8>3.3.co;2-3
72. Katayama, K., Takahashi, N., Ogawara, K., and Hattori, T. (1999). Pure topograph-ical disorientation due to right posterior cingulate lesion. Cortex 35, 279-282. doi: 10.1016/s0010-9452(08)70801-3
73. Katche, C., Bekinschtein, P., Slipczuk, L., Goldin, A., Izquierdo, I. A., Cammarota, M., et al. (2010). Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc. Natl. Acad. Sci. U S A 107, 349-354. doi: 10.1073/pnas.0912931107
74. Katche, C., Dorman, G., Gonzalez, C., Kramar, C. P., Slipczuk, L., Rossato, J. I., et al. (2013a). On the role of retrosplenial cortex in long-lasting memory storage. Hippocampus 23, 295-302. doi: 10.1002/hipo.22092
75. Katche, C., Dorman, G., Slipczuk, L., Cammarota, M., and Medina, J. H. (2013b). Functional integrity of the retrosplenial cortex is essential for rapid consoli-dation and recall of fear memory. Learn. Mem. 20, 170-173.doi: 10.1101/lm. 030080.112
76. Keene, C. S., and Bucci, D. J. (2008a). Contributions of the retrosplenial and posterior parietal cortices to cue-specific and contextual fear conditioning. Behav. Neurosci. 122, 89-97.doi: 10.1037/0735-7044.122.1.89
77. Keene, C. S., and Bucci, D. J. (2008b). Involvement of the retrosplenial cortex in processing multiple conditioned stimuli. Behav. Neurosci. 122, 651-658. doi: 10.1037/0735-7044.122.3.651
78. Keene, C. S., and Bucci, D. J. (2008c). Neurotoxic lesions of retrosplenial cortex disrupt signaled and unsignaled contextual fear conditioning. Behav. Neurosci. 122, 1070-1077. doi: 10.1037/a0012895
79. Keene, C. S., and Bucci, D. J. (2009). Damage to the retrosplenial cortex produces specific impairments in spatial working memory. Neurobiol. Learn. Mem. 91, 408-414. doi: 10.1016/j.nlm.2008.10.009
80. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256, 675-677. doi: 10.1126/science.1585183
81. Kobayashi, Y., and Amaral, D. G. (2003). Macaque monkey retrosplenial cortex: II. Cortical afferents. J. Comp. Neurol. 466, 48-79. doi: 10.1002/cne.10883
82. Kobayashi, Y., and Amaral, D. G. (2007). Macaque monkey retrosplenial cortex: III. Cortical efferents. J. Comp. Neurol. 502, 810-833. doi: 10.1002/cne.21346
83. Komorowski, R. W., Manns, J. R., and Eichenbaum, H. (2009). Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J. Neurosci. 29, 9918-9929. doi: 10.1523/JNEUROSCI.1378-09.2009
84. Kravitz, D. J., Saleem, K. S., Baker, C. I., and Mishkin, M. (2011). A new neural framework for visuospatial processing. Nat. Rev. Neurosci. 12, 217-230.doi: 10. 1038/nrn3008
85. Kubota, Y., and Gabriel, M. (1995). Studies of the limbic comparator: limbic circuit training-induced unit activity and avoidance behavior in rabbits with anterior dorsal thalamic lesions. Behav. Neurosci. 109, 258-277.doi: 10.1037//0735-7044. 109.2.258
86. Lavenex, P., Suzuki, W. A., and Amaral, D. G. (2002). Perirhinal and parahippocam-pal cortices of the macaque monkey: projections to the neocortex. J. Comp. Neurol. 447, 394-420.doi: 10.1002/cne.10243
87. Law, L. M., and Smith, D. M. (2012). The anterior thalamus is critical for over-coming interference in a context-dependent odor discrimination task. Behav. Neurosci. 126, 710-719. doi: 10.1037/a0029698
88. Leung, L. W., and Borst, J. G. (1987). Electrical activity of the cingulate cortex. I. Generating mechanisms and relations to behavior. Brain Res. 407, 68-80.doi: 10. 1016/0006-8993(87)91220-0
89. Levine, D. N., Warach, J., and Farah, M. (1985). Two visual systems in mental imagery: dissociation of what and where in imagery disorders due to bilateral posterior cerebral lesions. Neurology 35, 1010-1018.doi: 10.1212/WNL. 35.7.1010
90. Lustig, C., Snyder, A. Z., Bhakta, M., O'brien, K. C., Mcavoy, M., Raichle, M. E., et al. (2003). Functional deactivations: change with age and dementia of the Alzheimer type. Proc. Natl. Acad. Sci. U S A 100, 14504-14509.doi: 10. 1073/pnas.2235925100
91. Maguire, E. A. (2001). The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand. J. Psychol. 42, 225-238. doi: 10.1111/1467-9450.00233
92. Maguire, E. A., Nannery, R., and Spiers, H. J. (2006). Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 129, 2894-2907. doi: 10. 1093/brain/awl286
93. Mankin, E. A., Sparks, F. T., Slayyeh, B., Sutherland, R. J., Leutgeb, S., and Leutgeb, J. K. (2012). Neuronal code for extended time in the hippocampus. Proc. Natl. Acad. Sci. U S A 109, 19462-19467. doi: 10.1073/pnas.1214107109
94. Mason, M. F., Norton, M. I., Van Horn, J. D., Wegner, D. M., Grafton, S. T., and Macrae, C. N. (2007). Wandering minds: the default network and stimulus-independent thought. Science 315, 393-395. doi: 10.1126/science. 1131295
95. Maviel, T., Durkin, T. P., Menzaghi, F., and Bontempi, B. (2004). Sites of neocortical reorganization critical for remote spatial memory. Science 305, 96-99. doi: 10.1126/science.1098180
96. McClelland, J. L., McNaughton, B. L., and O'Reilly, R. C. (1995). 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. 102, 419-457. doi: 10.1037/0033-295x.102.3.419
97. Mizumori, S. J., Smith, D. M., and Puryear, C. B. (2007). Hippocampal and neocor-tical interactions during context discrimination: electrophysiological evidence from the rat. Hippocampus 17, 851-862. doi: 10.1002/hipo.20317
98. Morgan, L. K., Macevoy, S. P., Aguirre, G. K., and Epstein, R. A. (2011). Distances between real-world locations are represented in the human hippocampus. J. Neurosci. 31, 1238-1245. doi: 10.1523/JNEUROSCI.4667-10.2011
99. Morris, R., Petrides, M., and Pandya, D. N. (1999). Architecture and connections of retrosplenial area 30 in the rhesus monkey (Macaca mulatta). Eur. J. Neurosci. 11, 2506-2518. doi: 10.1046/j.1460-9568.1999.00672.x
100. Morris, R. G. (2006). Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci. 23, 2829-2846. doi: 10.1111/j.1460-9568.2006.04888.x
101. Moser, E. I., Kropff, E., and Moser, M B. (2008). Place cells, grid cells and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89. doi: 10. 1146/annurev.neuro.31.061307.090723
102. Nadel, L., Willner, J., and Kurz, E. M. (1985). Cognitive maps and environmental context, in Context and Learning, eds P. Balsam and A. Tomie (Hillsdale, NJ: Lawrence Erlbaum Associates), 385-406.
103. Nelson, A. J., Hindley, E. L., Haddon, J. E., Vann, S. D., and Aggleton, J. P. (2014). A novel role for the rat retrosplenial cortex in cognitive control. Learn. Mem. 21, 90-97. doi: 10.1101/lm.032136.113
104. Obi, T., Bando, M., Takeda, K., and Sakuta, M. (1992). A case of topographical disturbance following a left medial parieto-occipital lobe infarction. Rinsho Shinkeigaku 32, 426-429.
105. Oka, Y., Maeshima, S., Morita, S., Ishida, K., Kunimoto, K., Yoshida, M., et al. (2003). A case of amnesia caused by a subcortical hematoma in the left retrosplenial region. No Shinkei Geka 31, 289-295.
106. O'Keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175. doi: 10.1016/0006-8993(71)90358-1
107. Palmer, T. E. (1975). The effects of contextual scenes on the identification of objects. Mem. Cognit. 3, 519-526. doi: 10.3758/BF03197524
108. Park, S., Intraub, H., Yi, D. J., Widders, D., and Chun, M. M. (2007). Beyond the edges of a view: boundary extension in human scene-selective visual cortex. Neuron 54, 335-342. doi: 10.1016/j.neuron.2007.04.006
109. Parron, C., and Save, E. (2004). Comparison of the effects of entorhinal and retrosplenial cortical lesions on habituation, reaction to spatial and non-spatial changes during object exploration in the rat. Neurobiol. Learn. Mem. 82, 1-11. doi: 10.1016/s1074-7427(04)00043-7
110. Penick, S., and Solomon, P. R. (1991). Hippocampus, context and conditioning. Behav. Neurosci. 105, 611-617. doi: 10.1037/0735-7044.105.5.611
111. Perenin, M. T., and Vighetto, A. (1988). Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111(Pt. 3), 643-674. doi: 10.1093/brain/111.3.643
112. Phillips, R. G., and Ledoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285. doi: 10.1037/0735-7044.106.2.274
113. Poirier, G. L., and Aggleton, J. P. (2009). Post-surgical interval and lesion location within the limbic thalamus determine extent of retrosplenial cortex immediate-early gene hypoactivity. Neuroscience 160, 452-469. doi: 10.1016/j.neuroscience. 2009.02.021
114. Pothuizen, H. H., Aggleton, J. P., and Vann, S. D. (2008). Do rats with retrosplenial cortex lesions lack direction? Eur. J. Neurosci. 28, 2486-2498. doi: 10.1111/j. 1460-9568.2008.06550.x
115. Pothuizen, H. H., Davies, M., Aggleton, J. P., and Vann, S. D. (2010). Effects of selective granular retrosplenial cortex lesions on spatial working memory in rats. Behav. Brain Res. 208, 566-575. doi: 10.1016/j.bbr.2010.01.001
116. Raichle, M. E., Macleod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. USA98,676-682.doi:10.1073/pnas.98.2.676
117. Robinson, S., Keene, C. S., Iaccarino, H. F., Duan, D., and Bucci, D. J. (2011). Involvement of retrosplenial cortex in forming associations between multiple sensory stimuli. Behav. Neurosci. 125, 578-587. doi: 10.1037/a0024262.
118. Robinson, S., Poorman, C. E., Marder, T. J., and Bucci, D. J. (2012). Identification of functional circuitry between retrosplenial and postrhinal cortices during fear conditioning. J. Neurosci. 32, 12076-12086. doi: 10.1523/JNEUROSCI.2814-12.2012
119. Rudy, J. W., and Sutherland, R. J. (1995). Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5, 375-389. doi: 10.1002/hipo.450050502
120. Shulman, G. L., Fiez, J. A., Corbetta, M., Buckner, R. L., Miezin, F. M., Raichle, M. E., et al. (1997). Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 9, 648-663. doi: 10.1162/jocn.1997.9.5.648
121. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., and Buzsaki, G. (2008). Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697. doi: 10.1016/j.neuron.2008.09.014
122. Skaggs, W. E., McNaughton, B. L., Wilson, M. A., and Barnes, C. A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172. doi: 10.1002/(SICI)1098-1063(1996)6:2%3C149::AID-HIPO6%3E3.0.CO;2-K
123. Smith, D. M., and Bulkin, D. A. (2014). The form and function of hippocampal context representations. Neurosci. Biobehav. Rev. 40c, 52-61. doi: 10.1016/j.neubiorev.2014.01.005
124. Smith, D. M., Barredo, J., and Mizumori, S. J. (2012). Complimentary roles of the hippocampus and retrosplenial cortex in behavioral context discrimination. Hippocampus 22, 1121-1133. doi: 10.1002/hipo.20958
125. Smith, D. M., Freeman, J. H. Jr., Nicholson, D., and Gabriel, M. (2002). Limbic thalamic lesions, appetitively motivated discrimination learning and training-induced neuronal activity in rabbits. J. Neurosci. 22, 8212-8221.
126. Smith, D. M., and Mizumori, S. J. (2006a). Hippocampal place cells, con-text and episodic memory. Hippocampus 16, 716-729. doi: 10.1002/hipo. 20208
127. Smith, D. M., and Mizumori, S. J. (2006b). Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J. Neurosci. 26, 3154-3163. doi: 10.1523/jneurosci.3234-05.2006
128. Smith, D. M., Wakeman, D., Patel, J., and Gabriel, M. (2004). Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimina-tion learning in rabbits (Oryctolagus cuniculus). Behav. Neurosci. 118, 1225-1239. doi: 10.1037/0735-7044.118.6.1225
129. Spreng, R. N. (2012). The fallacy of a task-negative network. Front. Psychol. 3:145. doi: 10.3389/fpsyg.2012.00145
130. Spreng, R. N., Mar, R. A., and Kim, A. S. (2009). The common neural basis of utobiographical memory, prospection, navigation, theory of mind and the default mode: a quantitative meta-analysis. J. Cogn. Neurosci. 21, 489-510. doi: 10.1162/jocn.2008.21029
131. Squire, L. R. (2004). Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn. Mem. 82, 171-177. doi: 10.1016/j.nlm.2004. 06.005
132. Staresina, B. P., Alink, A., Kriegeskorte, N., and Henson, R. N. (2013). Awake reactivation predicts memory in humans. Proc. Natl. Acad. Sci. U S A 110, 21159-21164. doi: 10.1073/pnas.1311989110
133. Stark, M., Coslett, H. B., and Saffran, E. M. (1996). Impairment of an egocentric map of locations: implications for perception and action. Cogn. Neuropsychol. 13, 481-523. doi: 10.1080/026432996381908
134. Sutherland, R. J., and Rudy, J. W. (1989). Configural association theory: the role of the hippocampal formation in learning, memory and amnesia. Psychobiology 17, 129-144.
135. Suzuki, W. A., and Amaral, D. G. (1994). Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 14, 1856-1877.
136. Takahashi, N., Kawamura, M., Shiota, J., Kasahata, N., and Hirayama, K. (1997). Pure topographic disorientation due to right retrosplenial lesion. Neurology 49, 464-469. doi: 10.1212/wnl.49.2.464
137. Talk, A., Kang, E., and Gabriel, M. (2004). Independent generation of theta rhythm in the hippocampus and posterior cingulate cortex. Brain Res. 1015, 15-24. doi: 10.1016/j.brainres.2004.04.051
138. Thompson, L. T., and Best, P. J. (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. doi: 10.1016/0006-8993(90)90555-p
139. Tolman, E. C. (1948). Cognitive maps in rats and men. Psychol. Rev. 55, 189-208. doi: 10.1037/h0061626
140. Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., et al. (2007). Schemas and memory consolidation. Science 316, 76-82. doi: 10.1126/science.1135935
141. Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., et al. (2011). Schema-dependent gene activation and memory encoding in neocortex. Science 333, 891-895. doi: 10.1126/science.1205274
142. Ungerleider, L. G., and Mishkin, M. (1982). Two cortical visual systems, in Analysis of Visual Behaviour, eds D. J. Ingle, M. Goodale and R. J. W. Mansfield (Cambridge, MA: MIT Press), 549-586.
143. Valenstein, E., Bowers, D., Verfaellie, M., Heilman, K. M., Day, A., and Watson, R. T. (1987). Retrosplenial amnesia. Brain 110(Pt. 6), 1631-1646. doi: 10.1093/brain/110.6.1631
144. Vallar, G. (1998). Spatial hemineglect in humans. Trends Cogn. Sci. 2, 87-97. doi: 10. 1016/s1364-6613(98)01145-0
145. Van der Meer, M. A., and Redish, A. D. (2011). Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31, 2843-2854. doi: 10.1523/JNEUROSCI.4869-10.2011
146. Van Groen, T., and Wyss, J. M. (1990). Connections of the retrosplenial granular a cortex in the rat. J. Comp. Neurol. 300, 593-606. doi: 10.1002/cne.903000412
147. Van Groen, T., and Wyss, J. M. (1992). Connections of the retrosplenial dysgranular cortex in the rat. J. Comp. Neurol. 315, 200-216. doi: 10.1002/cne.903150207
148. Van Groen, T., and Wyss, J. M. (2003). Connections of the retrosplenial granular b cortex in the rat. J. Comp. Neurol. 463, 249-263. doi: 10.1002/cne.10757
149. Vann, S. D., Aggleton, J. P., and Maguire, E. A. (2009). What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792-802. doi: 10.1038/nrn2733
150. Vann, S. D., and Aggleton, J. P. (2002). Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. Behav. Neurosci. 116, 85-94. doi: 10.1037/0735-7044.116.1.85
151. Vogt, B. A. (1976). Retrosplenial cortex in the rhesus monkey: a cytoarchitectonic and Golgi study. J. Comp. Neurol. 169, 63-97. doi: 10.1002/cne.901690105
152. Vogt, B. A., and Laureys, S. (2005). Posterior cingulate, precuneal and retros-plenial cortices: cytology and components of the neural network correlates of consciousness. Prog. Brain Res. 150, 205-217. doi: 10.1016/s0079-6123(05) 50015-3
153. Vogt, B. A., Pandya, D. N., and Rosene, D. L. (1987). Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. J. Comp. Neurol. 262, 256-270. doi: 10.1002/cne.902620207
154. Wilson, M. A., and McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679. doi: 10.1126/science.8036517
155. Winocur, G., Moscovitch, M., Caruana, D. A., and Binns, M. A. (2005a). Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial mem-ory. Neuropsychologia 43, 1580-1590. doi: 10.1016/j.neuropsychologia.2005.01.013
156. Winocur, G., Moscovitch, M., Fogel, S., Rosenbaum, R. S., and Sekeres, M. (2005b). Preserved spatial memory after hippocampal lesions: effects of extensive expe-rience in a complex environment. Nat. Neurosci. 8, 273-275. doi: 10.1038/ nn1401
157. Winters, B. D., Forwood, S. E., Cowell, R. A., Saksida, L. M., and Bussey, T. J. (2004). Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: hetero-geneity of function within the temporal lobe. J. Neurosci. 24, 5901-5908. doi: 10. 1523/jneurosci.1346-04.2004
158. Wolbers, T., and Buchel, C. (2005). Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J. Neurosci. 25, 3333-3340. doi: 10.1523/jneurosci.4705-04.2005
159. Young, C. K., and McNaughton, N. (2009). Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb. Cortex 19, 24-40. doi: 10.1093/cercor/bhn055
160. Zanatta, M. S., Quillfeldt, J. H., Schaeffer, E., Schmitz, P. K., Quevedo, J., Medina, J. H., et al. (1997). Involvement of the hippocampus, amygdala, entorhinal cortex and posterior parietal cortex in memory consolidation. Braz. J. Med. Biol. Res. 30, 235-240. doi: 10.1590/s0100-879x1997000200012