Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2015, Article ID 414173, 9 pages
http://dx.doi.org/10.1155/2015/414173
Review Article

Retrosplenial Cortex and Long-Term Memory: Molecules to Behavior

Department of Psychological and Brain Sciences, Dartmouth College, Hanover 03755, NH, USA

Received 11 December 2014; Accepted 13 March 2015

Academic Editor: Jorge H. Medina

Copyright © 2015 Travis P. Todd and David J. Bucci. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. Bucci and S. Robinson, “Toward a conceptualization of retrohippocampal contributions to learning and memory,” Neurobiology of Learning and Memory, vol. 116, pp. 197–207, 2014. View at Publisher · View at Google Scholar
  2. C. Ranganath and M. Ritchey, “Two cortical systems for memory-guided behaviour,” Nature Reviews Neuroscience, vol. 13, no. 10, pp. 713–726, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. K. L. Agster and R. D. Burwell, “Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat,” Hippocampus, vol. 19, no. 12, pp. 1159–1186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. J. P. Aggleton, N. F. Wright, S. D. Vann, and R. C. Saunders, “Medial temporal lobe projections to the retrosplenial cortex of the macaque monkey,” Hippocampus, vol. 22, no. 9, pp. 1883–1900, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. R. D. Burwell and D. G. Amaral, “Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat,” The Journal of Comparative Neurology, vol. 398, no. 2, pp. 179–205, 1998. View at Publisher · View at Google Scholar
  6. Y. Kobayashi and D. G. Amaral, “Macaque monkey retrosplenial cortex: II. Cortical afferents,” Journal of Comparative Neurology, vol. 466, no. 1, pp. 48–79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Kobayashi and D. G. Amaral, “Macaque monkey retrosplenial cortex: III. Cortical efferents,” Journal of Comparative Neurology, vol. 502, no. 5, pp. 810–833, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Sugar, M. P. Witter, N. M. van Strien, and N. L. M. Cappaert, “The retrosplenial cortex: intrinsic connectivity and connections with the (para)hippocampal region in the rat. An interactive connectome,” Frontiers in Neuroinformatics, vol. 5, article 7, 2011. View at Publisher · View at Google Scholar
  9. T. van Groen and J. M. Wyss, “Connections of the retrosplenial granular a cortex in the rat,” Journal of Comparative Neurology, vol. 300, no. 4, pp. 593–606, 1990. View at Publisher · View at Google Scholar · View at Scopus
  10. T. van Groen and J. M. Wyss, “Connections of the retrosplenial dysgranular cortex in the rat,” Journal of Comparative Neurology, vol. 315, no. 2, pp. 200–216, 1992. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Van Groen and J. M. Wyss, “Connections of the retrosplenial granular b cortex in the rat,” Journal of Comparative Neurology, vol. 463, no. 3, pp. 249–263, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. T. van Groen and J. M. Wyss, “Projections from the laterodorsal nucleus of the thalamus to the limbic and visual cortices in the rat,” Journal of Comparative Neurology, vol. 324, no. 3, pp. 427–448, 1992. View at Publisher · View at Google Scholar · View at Scopus
  13. B. A. Vogt, D. N. Pandya, and D. L. Rosene, “Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents,” Journal of Comparative Neurology, vol. 262, no. 2, pp. 256–270, 1987. View at Publisher · View at Google Scholar · View at Scopus
  14. M. M. Jankowski, K. C. Ronnqvist, M. Tsanov et al., “The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation,” Frontiers in Systems Neuroscience, vol. 7, article 45, 2013. View at Publisher · View at Google Scholar
  15. S. D. Vann, J. P. Aggleton, and E. A. Maguire, “What does the retrosplenial cortex do?” Nature Reviews Neuroscience, vol. 10, no. 11, pp. 792–802, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. N. M. van Strien, N. L. M. Cappaert, and M. P. Witter, “The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network,” Nature Reviews Neuroscience, vol. 10, no. 4, pp. 272–282, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. J. P. Aggleton, “Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 7, pp. 1579–1596, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. M. D. Barense, T. J. Bussey, A. C. H. Lee et al., “Functional specialization in the human medial temporal lobe,” The Journal of Neuroscience, vol. 25, no. 44, pp. 10239–10246, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Eichenbaum, M. Sauvage, N. Fortin, R. Komorowski, and P. Lipton, “Towards a functional organization of episodic memory in the medial temporal lobe,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 7, pp. 1597–1608, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. S. C. Furtak, S.-M. Wei, K. L. Agster, and R. D. Burwell, “Functional neuroanatomy of the parahippocampal region in the rat: the perirhinal and postrhinal cortices,” Hippocampus, vol. 17, no. 9, pp. 709–722, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. R. Hunsaker, V. Chen, G. T. Tran, and R. P. Kesner, “The medial and lateral entorhinal cortex both contribute to contextual and item recognition memory: a test of the binding ofitems and context model,” Hippocampus, vol. 23, no. 5, pp. 380–391, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. B. P. Staresina, K. D. Duncan, and L. Davachi, “Perirhinal and parahippocampal cortices differentially contribute to later recollection of object- and scene-related event details,” Journal of Neuroscience, vol. 31, no. 24, pp. 8739–8747, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. S. Fanselow, “Contextual fear, gestalt memories, and the hippocampus,” Behavioural Brain Research, vol. 110, no. 1-2, pp. 73–81, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. J. H. Freeman Jr., C. Cuppernell, K. Flannery, and M. Gabriel, “Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits,” Behavioural Brain Research, vol. 80, no. 1-2, pp. 123–136, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. K. T. Harker and I. Q. Whishaw, “Impaired spatial performance in rats with retrosplenial lesions: importance of the spatial problem and the rat strain in identifying lesion effects in a swimming pool,” Journal of Neuroscience, vol. 22, no. 3, pp. 1155–1164, 2002. View at Google Scholar · View at Scopus
  26. K. T. Harker and I. Q. Whishaw, “A reaffirmation of the retrosplenial contribution to rodent navigation: reviewing the influences of lesion, strain, and task,” Neuroscience & Biobehavioral Reviews, vol. 28, no. 5, pp. 485–496, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. C. S. Keene and D. J. Bucci, “Contributions of the retrosplenial and posterior parietal cortices to cue-specific and contextual fear conditioning,” Behavioral Neuroscience, vol. 122, no. 1, pp. 89–97, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. C. S. Keene and D. J. Bucci, “Involvement of the retrosplenial cortex in processing multiple conditioned stimuli,” Behavioral Neuroscience, vol. 122, no. 3, pp. 651–658, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. C. S. Keene and D. J. Bucci, “Neurotoxic lesions of retrosplenial cortex disrupt signaled and unsignaled contextual fear conditioning,” Behavioral Neuroscience, vol. 122, no. 5, pp. 1070–1077, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. C. S. Keene and D. J. Bucci, “Damage to the retrosplenial cortex produces specific impairments in spatial working memory,” Neurobiology of Learning and Memory, vol. 91, no. 4, pp. 408–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Robinson, C. A. Poorman, T. J. Marder, and D. J. Bucci, “Identification of functional circuitry between retrosplenial and postrhinal cortices during fear conditioning,” Journal of Neuroscience, vol. 32, no. 35, pp. 12076–12086, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Robinson, C. S. Keene, H. F. Iaccarino, D. Duan, and D. J. Bucci, “Involvement of retrosplenial cortex in forming associations between multiple sensory stimuli,” Behavioral Neuroscience, vol. 125, no. 4, pp. 578–587, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. D. M. Smith, D. Wakeman, J. Patel, and M. Gabriel, “Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimination learning in rabbits (Oryctolagus cuniculus),” Behavioral Neuroscience, vol. 118, no. 6, pp. 1225–1239, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. D. M. Smith, J. Barredo, and S. J. Y. Mizumori, “Complimentary roles of the hippocampus and retrosplenial cortex in behavioral context discrimination,” Hippocampus, vol. 22, no. 5, pp. 1121–1133, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Talk, E. Stoll, and M. Gabriel, “Cingulate cortical coding of context-dependent latent inhibition,” Behavioral Neuroscience, vol. 119, no. 6, pp. 1524–1532, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. S. D. Vann and J. P. Aggleton, “Testing the importance of the retrosplenial guidance system: effects of different sized retrosplenial cortex lesions on heading direction and spatial working memory,” Behavioural Brain Research, vol. 155, no. 1, pp. 97–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Kubik, T. Miyashita, A. Kubik-Zahorodna, and J. F. Guzowski, “Loss of activity-dependent Arc gene expression in the retrosplenial cortex after hippocampal inactivation: interaction in a higher-order memory circuit,” Neurobiology of Learning and Memory, vol. 97, no. 1, pp. 124–131, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Wolbers and C. Büchel, “Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations,” The Journal of Neuroscience, vol. 25, no. 13, pp. 3333–3340, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. T. P. Todd, H. C. Meyer, and D. J. Bucci, “Contribution of the retrosplenial cortex to temporal discrimination learning,” Hippocampus, vol. 25, no. 2, pp. 137–141, 2015. View at Google Scholar
  40. M. E. Bouton, “Context, time, and memory retrieval in the interference paradigms of Pavlovian learning,” Psychological Bulletin, vol. 114, no. 1, pp. 80–99, 1993. View at Publisher · View at Google Scholar · View at Scopus
  41. M. E. Bouton, “Context, ambiguity, and unlearning: sources of relapse after behavioral extinction,” Biological Psychiatry, vol. 52, no. 10, pp. 976–986, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. M. E. Bouton, “The multiple forms of ‘context’ in associative learning theory,” in The Mind in Context, B. Mesquita, L. F. Barrent, and E. R. Smith, Eds., The Guilford Press, New York, NY, USA, 2010. View at Google Scholar
  43. J. M. Rosas and M. E. Bouton, “Context change and retention interval can have additive, rather than interactive, effects after taste aversion extinction,” Psychonomic Bulletin & Review, vol. 5, no. 1, pp. 79–83, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. E. A. Murray, T. J. Bussey, R. R. Hampton, and L. M. Saksida, “The parahippocampal region and object identification,” Annals of the New York Academy of Sciences, vol. 911, pp. 166–174, 2000. View at Google Scholar · View at Scopus
  45. W. J. Brogden, “Sensory pre-conditioning,” Journal of Experimental Psychology, vol. 25, no. 4, pp. 323–332, 1939. View at Publisher · View at Google Scholar · View at Scopus
  46. A. P. Blaisdell, K. J. Leising, W. D. Stahlman, and M. S. Waldmann, “Rats distinguish between absence of events and lack of information in sensory preconditioning,” International Journal of Comparative Psychology, vol. 22, pp. 1–18, 2009. View at Google Scholar
  47. P. C. Holland and R. T. Ross, “Savings test for associations between neutral stimuli,” Animal Learning & Behavior, vol. 11, no. 1, pp. 83–90, 1983. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Robinson, T. P. Todd, A. R. Pasternak et al., “Chemogenetic silencing of neurons in retrosplenial cortex disrupts sensory preconditioning,” Journal of Neuroscience, vol. 34, no. 33, pp. 10982–10988, 2014. View at Publisher · View at Google Scholar
  49. G. E. Wimmer and D. Shohamy, “Preference by association: how memory mechanisms in the hippocampus bias decisions,” Science, vol. 338, no. 6104, pp. 270–273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. M. D. Iordanova, M. Good, and R. C. Honey, “Retrieval-mediated learning involving episodes requires synaptic plasticity in the hippocampus,” Journal of Neuroscience, vol. 31, no. 19, pp. 7156–7162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. M. E. Fanselow, “Factors governing one-trial contextual conditioning,” Animal Learning & Behavior, vol. 18, no. 3, pp. 264–270, 1990. View at Publisher · View at Google Scholar · View at Scopus
  52. K. A. Corcoran, M. D. Donnan, N. C. Tronson et al., “NMDA receptors in retrosplenial cortex are necessary for retrieval of recent and remote context fear memory,” The Journal of Neuroscience, vol. 31, no. 32, pp. 11655–11659, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. E. Bouton and T. P. Todd, “A fundamental role for context in instrumental learning and extinction,” Behavioural Processes, vol. 104, pp. 13–19, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. S. J. Shettleworth, Cognition, Evolution, and Behavior, Oxford University Press, Oxford, UK, 2010.
  55. J. P. Aggleton and J. M. Pearce, “Neural systems underlying episodic memory: insights from animal research,” Philosophical Transactions of the Royal Society B, vol. 356, no. 1413, pp. 1467–1482, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. J. W. Rudy, “Context representations, context functions, and the parahippocampal-hippocampal system,” Learning & Memory, vol. 16, no. 10, pp. 573–585, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. M. P. Miller, L. C. Vedder, L. M. Law, and D. M. Smith, “Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition,” Frontiers in Human Neuroscience, vol. 8, article 586, 2014. View at Publisher · View at Google Scholar
  58. R. Czajkowski, B. Jayaprakash, B. Wiltgen et al., “Encoding and storage of spatial information in the retrosplenial cortex,” Proceedings of the National Academy of Sciences, vol. 111, no. 23, pp. 8661–8666, 2014. View at Publisher · View at Google Scholar
  59. A. Haijima and Y. Ichitani, “Anterograde and retrograde amnesia of place discrimination in retrosplenial cortex and hippocampal lesioned rats,” Learning & Memory, vol. 15, no. 7, pp. 477–482, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. R. C. O'Reilly and J. W. Rudy, “Conjunctive representations in learning and memory: principles of cortical and hippocampal function,” Psychological Review, vol. 108, no. 2, pp. 311–345, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. M. E. Bouton, “Context and behavioral processes in extinction,” Learning & Memory, vol. 11, no. 5, pp. 485–494, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. K. A. Corcoran, K. Leaderbrand, and J. Radulovic, “Extinction of remotely acquired fear depends on an inhibitory NR2B/PKA pathway in the retrosplenial cortex,” Journal of Neuroscience, vol. 33, no. 50, pp. 19492–19498, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. M. E. Bouton, R. F. Westbrook, K. A. Corcoran, and S. Maren, “Contextual and temporal modulation of extinction: behavioral and biological mechanisms,” Biological Psychiatry, vol. 60, no. 4, pp. 352–360, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. M. E. Bouton and R. C. Bolles, “Contextual control of the extinction of conditioned fear,” Learning and Motivation, vol. 10, no. 4, pp. 445–466, 1979. View at Publisher · View at Google Scholar · View at Scopus
  65. J. L. Kwapis, T. J. Jarome, J. L. Lee, M. R. Gilmartin, and F. J. Helmstetter, “Extinguishing trace fear engages the retrosplenial cortex rather than the amygdala,” Neurobiology of Learning and Memory, vol. 113, pp. 41–54, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. M. M. Albasser, G. L. Poirier, E. C. Warburton, and J. P. Aggleton, “Hippocampal lesions halve immediate-early gene protein counts in retrosplenial cortex: distal dysfunctions in a spatial memory system,” European Journal of Neuroscience, vol. 26, no. 5, pp. 1254–1266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. G. L. Poirier, K. L. Shires, D. Sugden et al., “Anterior thalamic lesions produce chronic and profuse transcriptional deregulation in retrosplenial cortex: a model of retrosplenial hypoactivity and covert pathology,” Thalamus and Related Systems, vol. 4, no. 1, pp. 59–77, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Amin, N. Wright, G. L. Poirier, K. L. Thomas, J. T. Erichsen, and J. P. Aggleton, “Selective lamina dysregulation in granular retrosplenial cortex (area 29) after anterior thalamic lesions: an in situ hybridization and trans-neuronal tracing study in rats,” Neuroscience, vol. 169, no. 3, pp. 1255–1267, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. J. R. Dumont, E. Amin, G. L. Poirier, M. M. Albasser, and J. P. Aggleton, “Anterior thalamic nuclei lesions in rats disrupt markers of neural plasticity in distal limbic brain regions,” Neuroscience, vol. 224, pp. 81–101, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. T. A. Jenkins, S. D. Vann, E. Amin, and J. P. Aggleton, “Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats?” European Journal of Neuroscience, vol. 19, no. 12, pp. 3291–3304, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. E. Knyihar-Csillik, Z. Chadaide, A. Mihaly, B. Krisztin-Peva, and B. Csillik, “Effect of electrical stimulation of the reticular nucleus of the rat thalamus upon c-fos immunoreactivity in the retrosplenial cortex,” Annals of Anatomy, vol. 187, no. 3, pp. 245–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Mendez-Lopez, J. L. Arias, B. Bontempi, and M. Wolff, “Reduced cytochrome oxidase activity in the retrosplenial cortex after lesions to the anterior thalamic nuclei,” Behavioural Brain Research, vol. 250, pp. 264–273, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. D. L. F. Garden, P. V. Massey, D. A. Caruana et al., “Anterior thalamic lesions stop synaptic plasticity in retrosplenial cortex slices: expanding the pathology of diencephalic amnesia,” Brain, vol. 132, no. 7, pp. 1847–1857, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Gabriel, R. W. Lambert, K. Foster, E. Orona, S. Sparenborg, and R. R. Maiorca, “Anterior thalamic lesions and neuronal activity in the cingulate and retrosplenial cortices during discriminative avoidance behavior in rabbits,” Behavioral Neuroscience, vol. 97, no. 5, pp. 675–696, 1983. View at Publisher · View at Google Scholar · View at Scopus
  75. J. R. Whitlock, A. J. Heynen, M. G. Shuler, and M. F. Bear, “Learning induces long-term potentiation in the hippocampus,” Science, vol. 313, no. 5790, pp. 1093–1097, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. B. C. Harland, D. A. Collings, N. McNaughton, W. C. Abraham, and J. C. Dalrymple-Alford, “Anterior thalamic lesions reduce spine density in both hippocampal CA1 and retrosplenial cortex, but enrichment rescues CA1 spines only,” Hippocampus, vol. 24, no. 10, pp. 1232–1247, 2014. View at Publisher · View at Google Scholar
  77. E. Ampuero, A. Dagnino-Subiabre, R. Sandoval et al., “Status epilepticus induces region-specific changes in dendritic spines, dendritic length and TrkB protein content of rat brain cortex,” Brain Research, vol. 1150, no. 1, pp. 225–238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Kasai, M. Fukuda, S. Watanabe, A. Hayashi-Takagi, and J. Noguchi, “Structural dynamics of dendritic spines in memory and cognition,” Trends in Neurosciences, vol. 33, no. 3, pp. 121–129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. P. Bekinschtein, M. Cammarota, and J. H. Medina, “BDNF and memory processing,” Neuropharmacology, vol. 76, pp. 677–683, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Maviel, T. P. Durkin, F. Menzaghi, and B. Bontempi, “Sites of neocortical reorganization critical for remote spatial memory,” Science, vol. 305, no. 5680, pp. 96–99, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. P. A. Gusev and A. N. Gubin, “Arc/arg3.1 mRNA global expression patterns elicited by memory recall in cerebral cortex differ for remote versus recent spatial memories,” Frontiers in Integrative Neuroscience, vol. 4, article 15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. P. J. Hernandez and T. Abel, “The role of protein synthesis in memory consolidation: progress amid decades of debate,” Neurobiology of Learning and Memory, vol. 89, no. 3, pp. 293–311, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Katche, G. Dorman, L. Slipczuk, M. Cammarota, and J. H. Medina, “Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory,” Learning & Memory, vol. 20, no. 4, pp. 170–173, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Katche, G. Dorman, C. Gonzalez et al., “On the role of retrosplenial cortex in long-lasting memory storage,” Hippocampus, vol. 23, no. 4, pp. 295–302, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. K. K. Cowansage, T. Shuman, B. C. Dillingham, A. Chang, P. Golshani, and M. Mayford, “Direct reactivation of a coherent neocortical memory of context,” Neuron, vol. 84, no. 2, pp. 432–441, 2014. View at Publisher · View at Google Scholar
  86. H. Shibata, Y. Honda, H. Sasaki, and J. Naito, “Organization of intrinsic connections of the retrosplenial cortex in the rat,” Anatomical Science International, vol. 84, no. 4, pp. 280–292, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Van Groen, I. Kadish, and J. M. Wyss, “Retrosplenial cortex lesions of area Rgb (but not of area Rga) impair spatial learning and memory in the rat,” Behavioural Brain Research, vol. 154, no. 2, pp. 483–491, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. S. D. Vann and J. P. Aggleton, “Selective dysgranular retrosplenial cortex lesions in rats disrupt allocentric performance of the radial-arm maze task,” Behavioral Neuroscience, vol. 119, no. 6, pp. 1682–1686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. H. H. J. Pothuizen, M. Davies, M. M. Albasser, J. P. Aggleton, and S. D. Vann, “Granular and dysgranular retrosplenial cortices provide qualitatively different contributions to spatial working memory: evidence from immediate-early gene imaging in rats,” European Journal of Neuroscience, vol. 30, no. 5, pp. 877–888, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. J. M. Rosas, T. P. Todd, and M. E. Bouton, “Context change and associative learning,” Wiley Interdisciplinary Reviews: Cognitive Science, vol. 4, no. 3, pp. 237–244, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, Calif, USA, 6th edition, 2007.