Table of Contents Author Guidelines Submit a Manuscript
Computational Intelligence and Neuroscience
Volume 2017 (2017), Article ID 8091780, 16 pages
https://doi.org/10.1155/2017/8091780
Research Article

Dorsoventral and Proximodistal Hippocampal Processing Account for the Influences of Sleep and Context on Memory (Re)consolidation: A Connectionist Model

1Department of Psychology, University of Arizona, Tucson, AZ 85721, USA
2Neuroscience Graduate Interdisciplinary Program, University of Arizona, Tucson, AZ 85721, USA
3Program in Applied Mathematics, University of Arizona, Tucson, AZ 85721, USA

Correspondence should be addressed to Jean-Marc Fellous; ude.anozira.liame@suollef

Received 13 February 2017; Revised 23 May 2017; Accepted 1 June 2017; Published 3 July 2017

Academic Editor: Jens Christian Claussen

Copyright © 2017 Justin Lines et al. 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. G. Buzsáki, “Neural syntax: cell assemblies, synapsembles, and readers,” Neuron, vol. 68, no. 3, pp. 362–385, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Nadel, “Memory formation, consolidation and transformation,” Neuroscience & Biobehavioral Reviews, vol. 36, no. 7, pp. 1640–1645, 2012. View at Google Scholar
  3. A. Besnard, J. Caboche, and S. Laroche, “Reconsolidation of memory: a decade of debate,” Progress in Neurobiology, vol. 99, no. 1, pp. 61–80, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. J. L. C. Lee, “Memory reconsolidation mediates the strengthening of memories by additional learning,” Nature Neuroscience, vol. 11, no. 11, pp. 1264–1266, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. L. C. Lee, “Reconsolidation: maintaining memory relevance,” Trends in Neurosciences, vol. 32, no. 8, pp. 413–420, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Nader and E. Ö. Einarsson, “Memory reconsolidation: an update,” Annals of the New York Academy of Sciences, vol. 1191, no. 1, pp. 27–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. N. C. Tronson and J. R. Taylor, “Molecular mechanisms of memory reconsolidation,” Nature Reviews Neuroscience, vol. 8, no. 4, pp. 262–275, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Hupbach, R. Gomez, O. Hardt, and L. Nadel, “Reconsolidation of episodic memories: a subtle reminder triggers integration of new information,” Learning and Memory, vol. 14, no. 1, pp. 47–53, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Hupbach, O. Hardt, R. Gomez, and L. Nadel, “The dynamics of memory: context-dependent updating,” Learning and Memory, vol. 15, no. 8, pp. 574–579, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Jones, E. Bukoski, L. Nadel, and J.-M. Fellous, “Remaking memories: reconsolidation updates positively motivated spatial memory in rats,” Learning and Memory, vol. 19, no. 3, pp. 91–98, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. B. J. Jones, S. M. Pest, I. M. Vargas, E. L. Glisky, and J.-M. Fellous, “Contextual reminders fail to trigger memory reconsolidation in aged rats and aged humans,” Neurobiology of Learning and Memory, vol. 120, pp. 7–15, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. A. S. Gupta, M. A. A. van der Meer, D. S. Touretzky, and A. D. Redish, “Hippocampal replay is not a simple function of experience,” Neuron, vol. 65, no. 5, pp. 695–705, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Ji and M. A. Wilson, “Coordinated memory replay in the visual cortex and hippocampus during sleep,” Nature Neuroscience, vol. 10, no. 1, pp. 100–107, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Wilson and B. L. McNaughton, “Reactivation of hippocampal ensemble memories during sleep,” Science, vol. 265, no. 5172, pp. 676–679, 1994. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Diekelmann and J. Born, “The memory function of sleep,” Nature Reviews Neuroscience, vol. 11, no. 2, pp. 114–126, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. K. A. Paller and J. L. Voss, “Memory reactivation and consolidation during sleep,” Learning and Memory, vol. 11, no. 6, pp. 664–670, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Stickgold, “Sleep-dependent memory consolidation,” Nature, vol. 437, no. 7063, pp. 1272–1278, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. J. M. Ellenbogen, J. C. Hulbert, R. Stickgold, D. F. Dinges, and S. L. Thompson-Schill, “Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference,” Current Biology, vol. 16, no. 13, pp. 1290–1294, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Peigneux, S. Laureys, S. Fuchs et al., “Are spatial memories strengthened in the human hippocampus during slow wave sleep?” Neuron, vol. 44, no. 3, pp. 535–545, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Yang, C. S. W. Lai, J. Cichon, L. Ma, W. Li, and W.-B. Gan, “Sleep promotes branch-specific formation of dendritic spines after learning,” Science, vol. 344, no. 6188, pp. 1173–1178, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. V. Ego-Stengel and M. A. Wilson, “Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat,” Hippocampus, vol. 20, no. 1, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Rasch, C. Büchel, S. Gais, and J. Born, “Odor cues during slow-wave sleep prompt declarative memory consolidation,” Science, vol. 315, no. 5817, pp. 1426–1429, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. J. D. Rudoy, J. L. Voss, C. E. Westerberg, and K. A. Paller, “Strengthening individual memories by reactivating them during sleep,” Science, vol. 326, no. 5956, p. 1079, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Oudiette and K. A. Paller, “Upgrading the sleeping brain with targeted memory reactivation,” Trends in Cognitive Sciences, vol. 17, no. 3, pp. 142–149, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Eichenbaum, “Hippocampus: cognitive processes and neural representations that underlie declarative memory,” Neuron, vol. 44, no. 1, pp. 109–120, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. J. O'Keefe and L. Nadel, The Hippocampus as A Cognitive Map, Clarendon Press, Oxford University Press, Oxford , NY, USA, 1978, 570 p.
  27. J. J. Knierim, J. P. Neunuebel, and S. S. Deshmukh, “Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames.,” Philosophical transactions of the Royal Society of London. Series B, Biological sciences, vol. 369, no. 1635, p. 20130369, 2014. View at Google Scholar · View at Scopus
  28. M. P. Witter and E. I. Moser, “Spatial representation and the architecture of the entorhinal cortex,” Trends in Neurosciences, vol. 29, no. 12, pp. 671–678, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Hafting, M. Fyhn, S. Molden, M.-B. Moser, and E. I. Moser, “Microstructure of a spatial map in the entorhinal cortex,” Nature, vol. 436, no. 7052, pp. 801–806, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Solstad, C. N. Boccara, E. Kropff, M.-B. Moser, and E. I. Moser, “Representation of geometric borders in the entorhinal cortex,” Science, vol. 322, no. 5909, pp. 1865–1868, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. E. L. Hargreaves, G. Rao, I. Lee, and J. J. Knierim, “Neuroscience: Major dissociation between medial and lateral entorhinal input to dorsal hippocampus,” Science, vol. 308, no. 5729, pp. 1792–1794, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Yoganarasimha, G. Rao, and J. J. Knierim, “Lateral entorhinal neurons are not spatially selective in cue-rich environments,” Hippocampus, vol. 21, no. 12, pp. 1363–1374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. J. P. Neunuebel and J. J. Knierim, “CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation,” Neuron, vol. 81, no. 2, pp. 416–427, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Treves and E. T. Rolls, “Computational analysis of the role of the hippocampus in memory,” Hippocampus, vol. 4, no. 3, pp. 374–391, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. R. P. Kesner, “Behavioral functions of the CA3 subregion of the hippocampus,” Learning and Memory, vol. 14, no. 11, pp. 771–781, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. R. P. Kesner and E. T. Rolls, “A computational theory of hippocampal function, and tests of the theory: new developments,” Neuroscience & Biobehavioral Reviews, vol. 48, no. 1, pp. 92–147, 2006. View at Google Scholar
  37. E. T. Rolls, “An attractor network in the hippocampus: theory and neurophysiology,” Learning and Memory, vol. 14, no. 11, pp. 714–731, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. E. J. Henriksen, L. L. Colgin, C. A. Barnes, M. P. Witter, M.-B. Moser, and E. I. Moser, “Spatial representation along the proximodistal axis of CA1,” Neuron, vol. 68, no. 1, pp. 127–137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Nakazawa, A. Pevzner, K. Z. Tanaka, and B. J. Wiltgen, “Memory retrieval along the proximodistal axis of CA1,” Hippocampus, vol. 26, no. 9, pp. 1140–1148, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Malik, K. A. Dougherty, K. Parikh, C. Byrne, and D. Johnston, “Mapping the electrophysiological and morphological properties of CA1 pyramidal neurons along the longitudinal hippocampal axis,” Hippocampus, vol. 26, no. 3, pp. 341–361, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. M.-B. Moser and E. I. Moser, “Functional differentiation in the hippocampus,” Hippocampus, vol. 8, no. 6, pp. 608–619, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Nadel, “Dorsal and ventral hippocampal lesions and behavior,” Physiology and Behavior, vol. 3, no. 6, pp. 891–900, 1968. View at Publisher · View at Google Scholar · View at Scopus
  43. R. W. Komorowski, C. G. Garcia, A. Wilson, S. Hattori, M. W. Howard, and H. Eichenbaum, “Ventral hippocampal neurons are shaped by experience to represent behaviorally relevant contexts,” Journal of Neuroscience, vol. 33, no. 18, pp. 8079–8087, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. R. W. Komorowski, J. R. Manns, and H. Eichenbaum, “Robust conjunctive item: place coding by hippocampal neurons parallels learning what happens where,” Journal of Neuroscience, vol. 29, no. 31, pp. 9918–9929, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Lyttle, B. Gereke, K. K. Lin, and J.-M. Fellous, “Spatial scale and place field stability in a grid-to-place cell model of the dorsoventral axis of the hippocampus,” Hippocampus, vol. 23, no. 8, pp. 729–744, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Greene, M. Howard, R. Bhattacharyya, and J.-M. Fellous, “Hippocampal anatomy supports the use of context in object recognition: a computational model,” Computational Intelligence and Neuroscience, vol. 2013, Article ID 294878, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Llofriu, G. Tejera, M. Contreras, T. Pelc, J. M. Fellous, and A. Weitzenfeld, “Goal-oriented robot navigation learning using a multi-scale space representation,” Neural Networks, vol. 72, pp. 62–74, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. R. C. O'Reilly, R. Bhattacharyya, M. D. Howard, and N. Ketz, “Complementary learning systems,” Cognitive Science, vol. 38, no. 6, pp. 1229–1248, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Nowicki, P. Verga, and H. Siegelmann, “Modeling reconsolidation in kernel associative memory,” PLoS ONE, vol. 8, no. 8, Article ID e68189, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. P. B. Sederberg, S. J. Gershman, S. M. Polyn, and K. A. Norman, “Human memory reconsolidation can be explained using the temporal context model,” Psychonomic Bulletin and Review, vol. 18, no. 3, pp. 455–468, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Malerba, G. P. Krishnan, J.-M. Fellous, and M. Bazhenov, “Hippocampal CA1 ripples as inhibitory transients,” PLoS Computational Biology, vol. 12, no. 4, Article ID e1004880, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Shen and B. L. McNaughton, “Modeling the spontaneous reactivation of experience-specific hippocampal cell assembles during sleep,” Hippocampus, vol. 6, no. 6, pp. 685–692, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. B. Aisa, B. Mingus, and R. O'Reilly, “The Emergent neural modeling system,” Neural Networks, vol. 21, no. 8, pp. 1146–1152, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. R. C. O'Reilly, The Leabra model of neural interactions and learning in the neocortex, Carnegie Mellon University, Pittsburgh, Pennsylvania, 1996.
  55. R. C. O'Reilly, “Biologically plausible error-driven learning using local activation differences: the generalized recirculation algorithm,” Neural Computation, vol. 8, no. 5, pp. 895–938, 1996. View at Publisher · View at Google Scholar · View at Scopus
  56. J. M. Ellenbogen, J. D. Payne, and R. Stickgold, “The role of sleep in declarative memory consolidation: passive, permissive, active or none?” Current Opinion in Neurobiology, vol. 16, no. 6, pp. 716–722, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. D. I. Schouten, S. I. R. Pereira, M. Tops, and F. M. Louzada, “State of the art on targeted memory reactivation: sleep your way to enhanced cognition,” Sleep Medicine Reviews, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. S. A. Cairney, S. Lindsay, J. M. Sobczak, K. A. Paller, and M. G. Gaskell, “The benefits of targeted memory reactivation for consolidation in sleep are contingent on memory accuracy and direct cue-memory associations,” Sleep, vol. 39, no. 5, pp. 1139–1150, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. R. S. Herz and T. Engen, “Odor memory: review and analysis,” Psychonomic Bulletin & Review, vol. 3, no. 3, pp. 300–313, 1996. View at Publisher · View at Google Scholar
  60. S. A. Josselyn, S. Köhler, and P. W. Frankland, “Finding the engram,” Nature Reviews Neuroscience, vol. 16, no. 9, pp. 521–534, 2015. View at Publisher · View at Google Scholar
  61. R. C. O'Reilly, “Six principles for biologically based computational models of cortical cognition,” Trends in Cognitive Sciences, vol. 2, no. 11, pp. 455–462, 1998. View at Publisher · View at Google Scholar · View at Scopus
  62. M. C. Anderson, “Rethinking interference theory: executive control and the mechanisms of forgetting,” Journal of Memory and Language, vol. 49, no. 4, pp. 415–445, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Groch, T. Schreiner, B. Rasch, R. Huber, and I. Wilhelm, “Prior knowledge is essential for the beneficial effect of targeted memory reactivation during sleep,” Scientific Reports, vol. 7, p. 39763, 2017. View at Publisher · View at Google Scholar
  64. A. E. Gold and R. P. Kesner, “The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat,” Hippocampus, vol. 15, no. 6, pp. 808–814, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Lavenex and P. Banta Lavenex, “Building hippocampal circuits to learn and remember: insights into the development of human memory,” Behavioural Brain Research, vol. 254, pp. 8–21, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. C. M. Lewis, A. Baldassarre, G. Committeri, G. L. Romani, and M. Corbetta, “Learning sculpts the spontaneous activity of the resting human brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17558–17563, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Nere, A. Hashmi, C. Cirelli, and G. Tononi, “Sleep-dependent synaptic down-selection (I): modeling the benefits of sleep on memory consolidation and integration,” Frontiers in Neurology, vol. 4, Article ID Article 143, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Tononi and C. Cirelli, “Sleep and synaptic homeostasis: a hypothesis,” Brain Research Bulletin, vol. 62, no. 2, pp. 143–150, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Tononi and C. Cirelli, “Sleep function and synaptic homeostasis,” Sleep Medicine Reviews, vol. 10, no. 1, pp. 49–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Bushey, G. Tononi, and C. Cirelli, “Sleep and synaptic homeostasis: structural evidence in Drosophila,” Science, vol. 332, no. 6037, pp. 1576–1581, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. K. B. Hengen, M. E. Lambo, S. D. van Hooser, D. B. Katz, and G. G. Turrigiano, “Firing rate homeostasis in visual cortex of freely behaving rodents,” Neuron, vol. 80, no. 2, pp. 335–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. W. Blanco, C. M. Pereira, V. R. Cota et al., “Synaptic homeostasis and restructuring across the sleep-wake cycle,” PLoS Computational Biology, vol. 11, no. 5, Article ID e1004241, 2015. View at Publisher · View at Google Scholar · View at Scopus
  73. W. Li, L. Ma, G. Yang, and W. Gan, “REM sleep selectively prunes and maintains new synapses in development and learning,” Nature Neuroscience, vol. 20, no. 3, pp. 427–437, 2017. View at Publisher · View at Google Scholar
  74. S. Ribeiro, V. Goyal, C. V. Mello, and C. Pavlides, “Brain gene expression during REM sleep depends on prior waking experience,” Learning and Memory, vol. 6, no. 5, pp. 500–508, 1999. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Ribeiro, C. V. Mello, T. Velho, T. J. Gardner, E. D. Jarvis, and C. Pavlides, “Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep,” Journal of Neuroscience, vol. 22, no. 24, pp. 10914–10923, 2002. View at Google Scholar · View at Scopus
  76. S. Diekelmann, J. Born, and U. Wagner, “Sleep enhances false memories depending on general memory performance,” Behavioural Brain Research, vol. 208, no. 2, pp. 425–429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. G. Buzsaki, “Two-stage model of memory trace formation: a role for ‘noisy’ brain states,” Neuroscience, vol. 31, no. 3, pp. 551–570, 1989. View at Publisher · View at Google Scholar · View at Scopus
  78. J. J. Chrobak and G. Buzsáki, “High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat,” Journal of Neuroscience, vol. 16, no. 9, pp. 3056–3066, 1996. View at Google Scholar · View at Scopus
  79. J. Shen, “Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience,” Journal of Sleep Research, vol. 7, no. 1, pp. 6–16, 1997. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Kloosterman, T. van Haeften, and F. H. Lopes da Silva, “Two reentrant pathways in the hippocampal-entorhinal system,” Hippocampus, vol. 14, no. 8, pp. 1026–1039, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. F. Kloosterman, T. Van Haeften, M. P. Witter, and F. H. Lopes Da Silva, “Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system,” European Journal of Neuroscience, vol. 18, no. 11, pp. 3037–3052, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Barbarosie and M. Avoli, “CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures,” Journal of Neuroscience, vol. 17, no. 23, pp. 9308–9314, 1997. View at Google Scholar · View at Scopus
  83. V. Gnatkovsky and M. De Curtis, “Hippocampus-mediated activation of superficial and deep layer neurons in the medial entorhinal cortex of the isolated guinea pig brain,” Journal of Neuroscience, vol. 26, no. 3, pp. 873–881, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. D. Pare, M. DeCurtis, and R. Llinas, “Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro,” Journal of Neuroscience, vol. 12, no. 5, pp. 1867–1881, 1992. View at Google Scholar · View at Scopus
  85. T. V. P. Bliss and G. L. Collingridge, “A synaptic model of memory: long-term potentiation in the hippocampus,” Nature, vol. 361, no. 6407, pp. 31–39, 1993. View at Publisher · View at Google Scholar · View at Scopus
  86. L. Ziegler, F. Zenke, D. B. Kastner, and W. Gerstner, “Synaptic consolidation: From synapses to behavioral modeling,” Journal of Neuroscience, vol. 35, no. 3, pp. 1319–1334, 2015. View at Publisher · View at Google Scholar · View at Scopus