Skip to main content
SpringerLink
Log in

Coordinated Sequence Replays Between the Visual Cortex and Hippocampus

  • Chapter
  • First Online:
Analysis and Modeling of Coordinated Multi-neuronal Activity

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 12))

Abstract

Based on our previously published study, in this chapter, we discuss the interaction between the hippocampus (CA1) and primary visual cortex (V1) in the acquisition and consolidation of memories with an emphasis upon how this study supports, and expands upon, contemporary memory theories. Both CA1 and V1 neurons were shown to contribute to the acquisition of hippocampal-dependent episodic memory and to the memory consolidation process during slow-wave sleep. V1 neurons also participate in hippocampal-independent remote memory function following consolidation. Thus, V1 neurons appear to be tuned to both external stimuli and internal memories. These data not only support key elements of contemporary memory theories but also provide fresh, new insights into the consolidation process. Our findings also raise important questions with regard to the distinctions between sensory and memory circuits.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992;99:195–231.

    Article  CAS  PubMed  Google Scholar 

  2. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry. 1957;20:11–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Corkin S. What’s new with the amnesic patient H.M.? Nat Rev Neurosci. 2002;3:153–60.

    Article  CAS  PubMed  Google Scholar 

  4. Marr D. A theory for cerebral neocortex. Proc R Soc Lond B Biol Sci. 1970;176(43):161–234.

    Article  CAS  PubMed  Google Scholar 

  5. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci. 1971;262(841):23–81.

    Article  CAS  PubMed  Google Scholar 

  6. McClelland JL, McNaughton BL, O’Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 1995;102:419–57.

    Article  CAS  PubMed  Google Scholar 

  7. Teyler TJ, Rudy JW. The hippocampal indexing theory and episodic memory: updating the index. Hippocampus. 2007;17:1158–69.

    Article  PubMed  Google Scholar 

  8. Buzsaki G. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31:551–70.

    Article  CAS  PubMed  Google Scholar 

  9. Buzsaki G. The hippocampo-neocortical dialogue. Cereb Cortex. 1996;6:81–92.

    Article  CAS  PubMed  Google Scholar 

  10. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, et al. Schemas and memory consolidation. Science. 2007;316(5821):76–82.

    Article  CAS  PubMed  Google Scholar 

  11. Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, et al. Schema-dependent gene activation and memory encoding in neocortex. Science. 2011;333(6044):891–5.

    Article  CAS  PubMed  Google Scholar 

  12. Teyler TJ, DiScenna P. The role of hippocampus in memory: a hypothesis. Neurosci Biobehav Rev. 1985;9(3):377–89.

    Article  CAS  PubMed  Google Scholar 

  13. Teyler TJ, DiScenna P. The hippocampal memory indexing theory. Behav Neurosci. 1986;100(2):147–54.

    Article  CAS  PubMed  Google Scholar 

  14. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171–5.

    Article  PubMed  Google Scholar 

  15. O’Keefe J. Place units in the hippocampus of the freely moving rat. Exp Neurol. 1976;51(1):78–109.

    Article  PubMed  Google Scholar 

  16. Itskov V, Curto C, Pastalkova E, Buzsáki G. Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J Neurosci. 2011;31(8):2828–34.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron. 2011;71(4):737–49.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Buzsáki G. Theta oscillations in the hippocampus. Neuron. 2002;33(3):325–40.

    Article  PubMed  Google Scholar 

  19. Wiltgen BJ, Brown RAM, Talton LE, Silva AJ. New circuits for old memories: the role of the neocortex in consolidation. Neuron. 2004;44(1):101–8.

    Article  CAS  PubMed  Google Scholar 

  20. Frankland PW, Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci. 2005;6:119–30.

    Article  CAS  PubMed  Google Scholar 

  21. Maviel T, Durkin TP, Menzaghi F, Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science. 2004;305(5680):96–9.

    Article  CAS  PubMed  Google Scholar 

  22. Takehara K, Kawahara S, Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci. 2003;23(30):9897–905.

    CAS  PubMed  Google Scholar 

  23. Lopez-Aranda MF, Lopez-Tellez JF, Navarro-Lobato I, Masmudi-Martin M, Gutierrez A, Khan ZU. Role of layer 6 of V2 visual cortex in object-recognition memory. Science. 2009;325:87–9.

    Article  CAS  PubMed  Google Scholar 

  24. Yao H, Shi L, Han F, Gao H, Dan Y. Rapid learning in cortical coding of visual scenes. Nat Neurosci. 2007;10:772–8.

    Article  CAS  PubMed  Google Scholar 

  25. Xu S, Jiang W, Poo MM, Dan Y. Activity recall in a visual cortical ensemble. Nat Neurosci. 2012;15:449–55, S1–2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Wheeler ME, Petersen SE, Buckner RL. Memory’s echo: vivid remembering reactivates sensory-specific cortex. Proc Natl Acad Sci U S A. 2000;97:11125–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, et al. The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science. 1999;284:167–70.

    Article  CAS  PubMed  Google Scholar 

  28. Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007;10:100–7.

    Article  CAS  PubMed  Google Scholar 

  29. 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. 1999;23:209–26.

    Article  CAS  PubMed  Google Scholar 

  30. Ferbinteanu J, Kennedy PJ, Shapiro ML. Episodic memory–from brain to mind. Hippocampus. 2006;16:691–703.

    Article  PubMed  Google Scholar 

  31. Knierim JJ, Lee I, Hargreaves EL. Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus. 2006;16:755–64.

    Article  PubMed  Google Scholar 

  32. McNaughton BL, Barnes CA, O’Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res. 1983;52:41–9.

    Article  CAS  PubMed  Google Scholar 

  33. Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261:1055–8.

    Article  CAS  PubMed  Google Scholar 

  34. Muller R. A quarter of a century of place cells. Neuron. 1996;17:813–22.

    Article  CAS  PubMed  Google Scholar 

  35. Muller RU, Kubie JL. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci. 1987;7:1951–68.

    CAS  PubMed  Google Scholar 

  36. Knierim JJ. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci. 2002;22:6254–64.

    CAS  PubMed  Google Scholar 

  37. Lee I, Yoganarasimha D, Rao G, Knierim JJ. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature. 2004;430:456–9.

    Article  CAS  PubMed  Google Scholar 

  38. Miller MW, Vogt BA. Direct connections of rat visual cortex with sensory, motor, and association cortices. J Comp Neurol. 1984;226:184–202.

    Article  CAS  PubMed  Google Scholar 

  39. Lavenex P, Amaral DG. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus. 2000;10:420–30.

    Article  CAS  PubMed  Google Scholar 

  40. Alvarez P, Squire LR. Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A. 1994;91:7041–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Kali S, Dayan P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci. 2004;7:286–94.

    Article  CAS  PubMed  Google Scholar 

  42. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ. An information-theoretic approach to deciphering the hippocampal code, Advances in neural processing systems. San Mateo: Morgan Kaufmann; 1993. p. 1030–7.

    Google Scholar 

  43. Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265:676–9.

    Article  CAS  PubMed  Google Scholar 

  44. Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36:1183–94.

    Article  CAS  PubMed  Google Scholar 

  45. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870–3.

    Article  CAS  PubMed  Google Scholar 

  46. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999;19:9497–507.

    CAS  PubMed  Google Scholar 

  47. Cossart R, Aronov D, Yuste R. Attractor dynamics of network UP states in the neocortex. Nature. 2003;423:283–8.

    Article  CAS  PubMed  Google Scholar 

  48. Shu Y, Hasenstaub A, McCormick DA. Turning on and off recurrent balanced cortical activity. Nature. 2003;423:288–93.

    Article  CAS  PubMed  Google Scholar 

  49. Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 2000;3:1027–34.

    Article  CAS  PubMed  Google Scholar 

  50. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A. 2003;100:13638–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Volgushev M, Chauvette S, Mukovski M, Timofeev I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations [corrected]. J Neurosci. 2006;26:5665–72.

    Article  CAS  PubMed  Google Scholar 

  52. Amzica F, Steriade M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience. 1998;82:671–86.

    Article  CAS  PubMed  Google Scholar 

  53. Steriade M, Timofeev I, Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol. 2001;85:1969–85.

    CAS  PubMed  Google Scholar 

  54. Hahn TT, Sakmann B, Mehta MR. Phase-locking of hippocampal interneurons’ membrane potential to neocortical up-down states. Nat Neurosci. 2006;9:1359–61.

    Article  CAS  PubMed  Google Scholar 

  55. Hahn TT, Sakmann B, Mehta MR. Differential responses of hippocampal subfields to cortical up-down states. Proc Natl Acad Sci U S A. 2007;104:5169–74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron. 2006;52:871–82.

    Article  CAS  PubMed  Google Scholar 

  57. Amzica F, Steriade M. Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J Neurosci. 1995;15(6):4658–77.

    CAS  PubMed  Google Scholar 

  58. Amzica F, Steriade M. Short- and long-range neuronal synchronization of the slow (<1 Hz) cortical oscillation. J Neurophysiol. 1995;73(1):20–38.

    CAS  PubMed  Google Scholar 

  59. Steriade M, Amzica F. Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J Sleep Res. 1998;7 Suppl 1:30–5.

    Article  PubMed  Google Scholar 

  60. Harris JA, Petersen RS, Diamond ME. The cortical distribution of sensory memories. Neuron. 2001;30:315–8.

    Article  CAS  PubMed  Google Scholar 

  61. MacLean JN, Watson BO, Aaron GB, Yuste R. Internal dynamics determine the cortical response to thalamic stimulation. Neuron. 2005;48:811–23.

    Article  CAS  PubMed  Google Scholar 

  62. Luczak A, Barthó P, Marguet SL, Buzsáki G, Harris KD. Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A. 2007;104(1):347–52.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Luczak A, Bartho P, Harris KD. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron. 2009;62:413–25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Girman SV, Sauve Y, Lund RD. Receptive field properties of single neurons in rat primary visual cortex. J Neurophysiol. 1999;82:301–11.

    CAS  PubMed  Google Scholar 

  65. Niell CM, Stryker MP. Highly selective receptive fields in mouse visual cortex. J Neurosci. 2008;28:7520–36.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Niell CM, Stryker MP. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron. 2010;65:472–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Olshausen BA, Field DJ. What is the other 85% of V1 doing? In: Sejnowski TJ, van Hemmen L, editors. Problems in systems neuroscience. Oxford: Oxford University Press; 2004.

    Google Scholar 

  68. Lee TS, Yang CF, Romero RD, Mumford D. Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency. Nat Neurosci. 2002;5:589–97.

    Article  CAS  PubMed  Google Scholar 

  69. Gilbert CD, Sigman M. Brain states: top-down influences in sensory processing. Neuron. 2007;54:677–96.

    Article  CAS  PubMed  Google Scholar 

  70. Gregoriou GG, Gotts SJ, Zhou H, Desimone R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science. 2009;324:1207–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Shuler MG, Bear MF. Reward timing in the primary visual cortex. Science. 2006;311:1606–9.

    Article  CAS  PubMed  Google Scholar 

  72. Vaudano E, Legg CR, Glickstein M. Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur J Neurosci. 1991;3:317–30.

    Article  PubMed  Google Scholar 

  73. Furtak SC, Wei SM, Agster KL, Burwell RD. Functional neuroanatomy of the parahippocampal region in the rat: the perirhinal and postrhinal cortices. Hippocampus. 2007;17:709–22.

    Article  PubMed  Google Scholar 

  74. Rolls ET. Hippocampo-cortical and cortico-cortical backprojections. Hippocampus. 2000;10:380–8.

    Article  CAS  PubMed  Google Scholar 

  75. Insausti R, Herrero MT, Witter MP. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus. 1997;7:146–83.

    Article  CAS  PubMed  Google Scholar 

  76. Burwell RD, Amaral DG. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol. 1998;398:179–205.

    Article  CAS  PubMed  Google Scholar 

  77. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Amsterdam: Elsevier; 2007.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, BCMT-T728, Houston, TX, 77030, USA

    Daniel Christopher Haggerty Ph.D. (Neuroscience) & Daoyun Ji Ph.D. (Neuroscience)

Authors
  1. Daniel Christopher Haggerty Ph.D. (Neuroscience)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daoyun Ji Ph.D. (Neuroscience)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daoyun Ji Ph.D. (Neuroscience) .

Editor information

Editors and Affiliations

  1. The University of Lethbridge, Lethbridge, Alberta, Canada

    Masami Tatsuno

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Haggerty, D.C., Ji, D. (2015). Coordinated Sequence Replays Between the Visual Cortex and Hippocampus. In: Tatsuno, M. (eds) Analysis and Modeling of Coordinated Multi-neuronal Activity. Springer Series in Computational Neuroscience, vol 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1969-7_9

Download citation

Publish with us

Policies and ethics

Search

Navigation