Skip to main content
SpringerLink
Log in

Hippocampal Sequences and the Cognitive Map

  • 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

Ensemble activity in the hippocampus is often arranged in temporal sequences of spiking. Early theoretical and experimental work strongly suggested that hippocampal sequences functioned as a neural mechanism for memory consolidation, and recent experiments suggest a causal link between sequences during sleep and mnemonic processing. However, in addition to sleep, the hippocampus expresses sequences during active behavior and moments of waking rest; recent data suggest that sequences outside of sleep might fulfill functions other than memory consolidation. These findings suggest a model in which sequence function varies depending on the neurophysiological and behavioral context in which they occur. In this chapter, we argue that hippocampal sequences are well suited to play roles in the formation, augmentation, and maintenance of a cognitive map. Specifically, we consider three postulated cognitive map functions (memory, construction of representations, and planning) and review data implicating hippocampal sequences in these processes. We conclude with a discussion of unanswered questions related to sequences and cognitive map function and highlight directions for future research.

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

Notes

  1. 1.

    The hippocampus is divided into multiple anatomical subfields [6], with the majority of place cell recordings deriving from the CA1 and CA3 regions. These regions exhibit interesting differences in both efferent and afferent connectivity [1]. In this chapter, we do not focus on these differences, but instead consider sequences recorded in both regions.

  2. 2.

    Recent evidence [73] suggests that backward LIA-associated sequences are present during sleep as well (albeit to a lesser extent than forward-ordered representations), suggesting that in some cases a similar problem with directional ambiguity could occur during off-line consolidation. Alternatively, this might suggest that both consolidation and constructive processes coexist during slow-wave sleep [79, 80].

References

  1. O’Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford: Clarendon; 1978.

    Google Scholar 

  2. Redish AD. Beyond the cognitive map: from place cells to episodic memory. Cambridge, MA: MIT Press; 1999.

    Google Scholar 

  3. Sutherland GR, McNaughton BL. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol. 2000;10(2):180–6.

    CAS  PubMed  Google Scholar 

  4. Carr MF, Jadhav SP, Frank LM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14(2):147–53.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Buhry L, Azizi AH, Cheng S. Reactivation, replay and preplay: how it might all fit together. Neural Plast. 2011;2011:1–11.

    Google Scholar 

  6. Lorento do Nó R. Studies on the structure of the cerebral cortex II. Continuation of the study of the ammonic system. J Psychol Neurol. 1934;46:113–77.

    Google Scholar 

  7. Green J, Arduini A. Hippocampal electrical activity in arousal. J Neurophysiol. 1954;17:531–57.

    Google Scholar 

  8. Vanderwolf CH. Limbic-diencephalic mechanisms of voluntary movement. Psychol Rev. 1971;78(2):83–113.

    CAS  PubMed  Google Scholar 

  9. Buzsáki G, Leung LW, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983;287(2):139–71.

    PubMed  Google Scholar 

  10. Buzsáki G. Rhythms of the brain. Oxford: Oxford University Press; 2006.

    Google Scholar 

  11. Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19(10):4090–101.

    CAS  PubMed  Google Scholar 

  12. Foster DJ, Wilson MA. Hippocampal theta sequences. Hippocampus. 2007;17:1093–9.

    PubMed  Google Scholar 

  13. Vanderwolf C. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol. 1969;26:407–18.

    CAS  PubMed  Google Scholar 

  14. Kramis R, Vanderwolf C, Bland B. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol. 1975;49:58–85.

    CAS  PubMed  Google Scholar 

  15. O’Keefe J, Recce M. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993;3:317–30.

    PubMed  Google Scholar 

  16. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus. 1996;6(2):149–73.

    CAS  PubMed  Google Scholar 

  17. Dragoi G, Buzsaki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron. 2006;50(1):145–57.

    CAS  PubMed  Google Scholar 

  18. Gupta A, van der Meer M, Touretzky D, Redish A. Segmentation of spatial experience by hippocampal θ sequences. Nat Neurosci. 2012;15:1032–9.

    CAS  PubMed  Google Scholar 

  19. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragol G, Czurkó A, et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature. 2002;417:738–41.

    CAS  PubMed  Google Scholar 

  20. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G. Internally generated cell assembly sequences in the rat hippocampus. Science. 2008;321(5894):1322–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Lenck-Santini PP, Fenton AA, Muller RU. Discharge properties of hippocampal neurons during performance of a jump avoidance task. J Neurosci. 2008;28(27):6773–86.

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Takahashi M, Lauwereyns J, Sakurai Y, Tsukada M. A code for spatial alternation during fixation in rat hippocampal CA1 neurons. J Neurophysiol. 2009;102(1):556–67.

    PubMed  Google Scholar 

  23. Buzsáki G. The “where is it?” reflex: autoshaping the orienting response. J Exp Anal Behav. 1982;37(3):461–84.

    PubMed Central  PubMed  Google Scholar 

  24. Buzsáki G. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31(3):551–70.

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  27. Nádasdy Z, Hirase H, Czurkó A, Csicsvari J, Buzsáki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999;19(2):9497–507.

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  29. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440(7084):680–3.

    CAS  PubMed  Google Scholar 

  30. O’Neill J, Senior T, Csicsvari J. Place-selective firing of ca1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006;49:143–55.

    PubMed  Google Scholar 

  31. Jackson JC, Johnson A, Redish AD. Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J Neurosci. 2006;26:12415–26.

    CAS  PubMed  Google Scholar 

  32. Diba K, Buzsáki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci. 2007;10:1241–2.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Tolman EC. Purposive behavior in animals and men. New York: Appleton Century-Crofts; 1932.

    Google Scholar 

  34. Tolman EC. The determiners of behavior at a choice point. Psychol Rev. 1938;45(1):1–41.

    Google Scholar 

  35. Tolman EC. Prediction of vicarious trial and error by means of the schematic sowbug. Psychol Rev. 1939;46:318–36.

    Google Scholar 

  36. Tolman EC, Ritchie BF, Kalish D. Studies in spatial learning I. Orientation and the short-cut. J Exp Psychol. 1946;36:13–24.

    CAS  PubMed  Google Scholar 

  37. Tolman EC. Cognitive maps in rats and men. Psychol Rev. 1948;55:189–208.

    CAS  PubMed  Google Scholar 

  38. Johnson A, Crowe D. Revisiting tolman: theories and cognitive maps. Cogn Critique. 2009;1(1):43–72.

    Google Scholar 

  39. Hull CL. Principles of behavior. New York: Appleton; 1943.

    Google Scholar 

  40. Guthrie ER. The psychology of learning (revised edition). New York: Harpers; 1952.

    Google Scholar 

  41. Tulving E, Madigan S. Memory and verbal learning. Annu Rev Psychol. 1970;21:437–84.

    Google Scholar 

  42. Hassabis D, Maguire E. The construction system of the brain. Philos Trans R Soc Lond B Biol Sci. 2009;364(1521):1263–71.

    PubMed Central  PubMed  Google Scholar 

  43. Schacter D, Addis D. On the nature of medial temporal lobe contributions to the constructive simulation of future events. Philos Trans R Soc Lond B Biol Sci. 2009;364(1521):1245.

    PubMed Central  PubMed  Google Scholar 

  44. Suddendorf T, Busby J. Mental time travel in animals? Trends Cogn Sci. 2003;7(9):391–6.

    PubMed  Google Scholar 

  45. Corballis M. Mental time travel: a case for evolutionary continuity. Trends Cogn Sci. 2012;17:5–6.

    PubMed  Google Scholar 

  46. Suddendorf M, Corballis M. The evolution of foresight: what is mental time travel, and is it unique to humans? Behav Brain Sci. 2007;30:299–312.

    PubMed  Google Scholar 

  47. Suddendorf T, Corballis MC. Behavioural evidence for mental time travel in nonhuman animals. Behav Brain Res. 2010;215:292–8.

    PubMed  Google Scholar 

  48. Lisman J, Redish AD. Prediction, sequences and the hippocampus. Philos Trans R Soc Lond B Biol Sci. 2009;364:1193–201.

    PubMed Central  PubMed  Google Scholar 

  49. Addis D, Schacter D. The hippocampus and imagining the future: where do we stand? Front Hum Neurosci. 2012;5:173.

    PubMed Central  PubMed  Google Scholar 

  50. Samsonovich AV, Ascoli GA. A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval. Learn Mem. 2005;12(2):193–208.

    PubMed Central  PubMed  Google Scholar 

  51. Hassabis D, Kumaran D, Vann SD, Maguire EA. Patients with hippocampal amnesia cannot imagine new experiences. Proc Natl Acad Sci U S A. 2007;104:1726–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Hassabis D, Kumaran D, Maguire E. Using imagination to understand the neural basis of episodic memory. J Neurosci. 2007;27:14365–74.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Buckner R. The role of the hippocampus in prediction and imagination. Annu Rev Psychol. 2010;61:27–48.

    PubMed  Google Scholar 

  54. Cohen NJ, Eichenbaum H. Memory, amnesia, and the hippocampal system. Cambridge, MA: MIT Press; 1993.

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  56. Hasselmo ME, Bower JM. Acetylcholine and memory. Trends Neurosci. 1993;16(6):218–22.

    CAS  PubMed  Google Scholar 

  57. Hasselmo ME. Acetylcholine and learning in a cortical associative memory. Neural Comput. 1993;5:32–44.

    Google Scholar 

  58. 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  59. Redish AD, Touretzky DS. The role of the hippocampus in solving the Morris water maze. Neural Comput. 1998;10(1):73–111.

    CAS  PubMed  Google Scholar 

  60. Squire LR, Zola-Morgan SM. The medial temporal lobe memory system. Science. 1991;253:1380–6.

    CAS  PubMed  Google Scholar 

  61. Dudai Y, Eisenberg M. Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron. 2004;44(1):93–100.

    CAS  PubMed  Google Scholar 

  62. O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010;33:220–9.

    PubMed  Google Scholar 

  63. Girardeau G, Zugaro M. Hippocampal ripples and memory consolidation. Curr Opin Neurobiol. 2011;21:452–9.

    CAS  PubMed  Google Scholar 

  64. Pavlides C, Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989;9(8):2907–18.

    CAS  PubMed  Google Scholar 

  65. Gerrard JL, Burke SN, McNaughton BL, Barnes CA. Sequence reactivation in the hippocampus is impaired in aged rats. J Neurosci. 2008;28:7883–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  66. Girardeau G, Benchenane K, Wiener SI, Buzs’aki G, Zugaro MB. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 2009;12:1222–3.

    CAS  PubMed  Google Scholar 

  67. Ego-Stengel V, Wilson MA. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus. 2010;20(1):1–10.

    PubMed Central  PubMed  Google Scholar 

  68. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus. 1996;6(3):271–80.

    CAS  PubMed  Google Scholar 

  69. Jensen O, Lisman JE. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem. 1996;3(23):279–87.

    CAS  PubMed  Google Scholar 

  70. Maurer AP, Burke SN, Lipa P, Skaggs WE, Barnes CA. Greater running speeds result in altered hippocampal phase sequence dynamics. Hippocampus. 2012;22(4):737–47.

    PubMed Central  PubMed  Google Scholar 

  71. Bieri KW, Bobbitt KN, Colgin LL. Slow and fast gamma rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron. 2014;82:670–81.

    CAS  PubMed  Google Scholar 

  72. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature. 2009;462(7271):353–7.

    CAS  PubMed  Google Scholar 

  73. Wikenheiser AM, Redish AD. The balance of forward and backward hippocampal sequences shifts across behavioral states. Hippocampus. 2013;23(1):22–9.

    PubMed Central  PubMed  Google Scholar 

  74. Karlsson MP, Frank LM. Awake replay of remote experiences in the hippocampus. Nat Neurosci. 2009;12:913–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Davidson TJ, Kloosterman F, Wilson MA. Hippocampal replay of extended experience. Neuron. 2009;63:497–507.

    CAS  PubMed  Google Scholar 

  76. Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. Hippocampal replay is not a simple function of experience. Neuron. 2010;65(5):695–705.

    CAS  PubMed  Google Scholar 

  77. Cheng S, Frank LM. New experiences enhance coordinated neural activity in the hippocampus. Neuron. 2008;57:303–13.

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Singer AC, Frank LM. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron. 2009;64(6):910–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Lewis PA, Durrant SJ. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn Sci. 2011;15:343–51.

    PubMed  Google Scholar 

  80. Stickgold R, Walker M. Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci. 2013;16:139–45.

    CAS  PubMed  Google Scholar 

  81. Derdikman D, Moser MB. A dual role for hippocampal replay. Neuron. 2010;65(5):582–4.

    CAS  PubMed  Google Scholar 

  82. Peters J, Büchel C. Episodic future thinking reduces reward delay discounting through an enhancement of prefrontal-mediotemporal interactions. Neuron. 2010;66(1):138–48.

    CAS  PubMed  Google Scholar 

  83. Johnson A, van der Meer MAA, Redish AD. Integrating hippocampus and striatum in decision-making. Curr Opin Neurobiol. 2007;17(6):692–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. van der Meer MAA, Redish AD. Expectancies in decision making, reinforcement learning, and ventral striatum. Front Neurosci. 2010;4:6.

    PubMed Central  PubMed  Google Scholar 

  85. Johnson A, Redish AD. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci. 2007;27(45):12176–89.

    CAS  PubMed  Google Scholar 

  86. Levy WB, Hocking AB, Wu XB. Interpreting hippocampal function as recoding and forecasting. Neural Netw. 2005;18:1242–64.

    PubMed  Google Scholar 

  87. Gill PR, Mizumori SJ, Smith DM. Hippocampal episode fields develop with learning. Hippocampus. 2011;21(11):1240–9.

    PubMed Central  PubMed  Google Scholar 

  88. 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  89. Eichenbaum H. Memory on time. Trends Cogn Sci. 2013;17(2):81–8.

    PubMed Central  PubMed  Google Scholar 

  90. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G. Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci. 2006;9:1526–33.

    CAS  PubMed  Google Scholar 

  91. Robbe D, Buzsaki G. Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J Neurosci. 2009;29(40):12597–605.

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Papale A, Stott J, Powell N, Regier P, Redish A. Interactions between deliberation and delay-discounting in rats. Cogn Affect Behav Neurosci. 2012;12:513–26.

    PubMed Central  PubMed  Google Scholar 

  93. Dragoi G, Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature. 2011;469:397–401.

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Rowland D, Yanovich Y, Kentros C. A stable hippocampal representation of a space requires its direct experience. Proc Natl Acad Sci U S A. 2011;108:14654–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Levcik D, Nekovarova T, Stuchlik A, Klement D. Rats use hippocampus to recognize positions of objects located in an inaccessible space. Hippocampus. 2013;23:153–61.

    CAS  PubMed  Google Scholar 

  96. Johnson A, Redish AD. Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model. Neural Netw. 2005;18(9):1163–71.

    PubMed  Google Scholar 

  97. Foster D, Knierim J. Sequence learning and the role of the hippocampus in rodent navigation. Curr Opin Neurobiol. 2012;22:294–300.

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Jadhav S, Kemere C, German P, Frank L. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2013;336:1454–8.

    Google Scholar 

  99. Kim S, Frank L. Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS One. 2009;4:e5494.

    PubMed Central  PubMed  Google Scholar 

  100. Pfeiffer B, Foster D. Hippocampal place-cell sequences depict future paths to remembered goals. Nature. 2013;497(7447):74–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Stevens R, Cowey A. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol. 1977;172:49–84.

    Google Scholar 

  102. Vann S, Brown M, Erichsen J, Aggleton J. Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. J Neurosci. 2000;20:2711–8.

    CAS  PubMed  Google Scholar 

  103. Nadel L. Dorsal and ventral hippocampal lesions and behavior. Physiol Behav. 2012;3:891–900.

    Google Scholar 

  104. Stevens R, Cowey A. Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation, and probably learning in rats. Brain Res. 1973;52:203–24.

    CAS  PubMed  Google Scholar 

  105. Moser E, Moser M, Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci. 1993;13:3916–25.

    CAS  PubMed  Google Scholar 

  106. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JNP. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci. 1999;113(6):1170–88.

    CAS  PubMed  Google Scholar 

  107. Richmond MA, Yee BK, Pouzet B, Veenman L, Rawlins JNP, Feldon J, et al. Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci. 1999;113(6):1189–203.

    CAS  PubMed  Google Scholar 

  108. Kjelstrup K, Tuvnes F, Steffenach H, Murison R, Moser E, Moser M. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A. 2002;99:10825–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, et al. Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev. 2004;28:273–83.

    CAS  PubMed  Google Scholar 

  110. Moser M, Moser E. Functional differentiation in the hippocampus. Hippocampus. 1998;8:608–19.

    CAS  PubMed  Google Scholar 

  111. Fanselow M, Dong H. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010;65:7–19.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Jung MW, Wiener SI, McNaughton BL. Comparison of spatial firing characteristics of the dorsal and ventral hippocampus of the rat. J Neurosci. 1994;14(12):7347–56.

    CAS  PubMed  Google Scholar 

  113. Poucet B, Thinus-Blanc C, Muller RU. Place cells in the ventral hippocampus of rats. Neuroreport. 1994;5(16):2045–8.

    CAS  PubMed  Google Scholar 

  114. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, et al. Finite scale of spatial representation in the hippocampus. Science. 2008;321(5885):140–3.

    CAS  PubMed  Google Scholar 

  115. Royer S, Sirota A, Patel J, Buzsaki G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci. 2010;30(5):1777–87.

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Malhorta S, Cross R, van der Meer M. Functional differentiation in the hippocampus. Rev Neurosci. 2012;23:39–65.

    Google Scholar 

  117. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER. Increased attention to spatial context increases both place field stability and spatial memory. Neuron. 2004;42:283–95.

    CAS  PubMed  Google Scholar 

  118. Adhikari A, Topiwala MA, Gordon JA. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron. 2010;28(65):2.

    Google Scholar 

  119. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10:49–62.

    PubMed  Google Scholar 

  120. Carr M, Frank L. A single microcircuit with multiple functions: state dependent information processing in the hippocampus. Curr Opin Neurobiol. 2012;22:704–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Nokia M, Penttonen M, Wikgren J. Hippocampal ripple-contingent training accelerates trace eyeblink conditioning and retards extinction in rabbits. J Neurosci. 2010;30:11486–92.

    CAS  PubMed  Google Scholar 

  122. Bendor D, Wilson M. Biasing the content of hippocampal replay during sleep. Nat Neurosci. 2012;15:1439–44.

    CAS  PubMed  Google Scholar 

  123. DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, et al. Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci U S A. 2007;104(13):5644–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Tort A, Kramer M, Thorn C, Gibson D, Kubota Y, Graybiel A, et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a t-maze task. Proc Natl Acad Sci U S A. 2008;105:20517–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  125. Benchenane K, Peyrache A, Khamassi M, Tierny PL, Gioanni Y, Battaglia FP, et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron. 2010;66(6):921–36.

    CAS  PubMed  Google Scholar 

  126. Colgin L. Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol. 2011;21:467–74.

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Gordon J. Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol. 2011;21:486–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Tort A, Scheffer-Teixeira R, Souza B, Draguhn A, Brankack J. Theta-associated high-frequency oscillations (110–160hz) in the hippocampus and neocortex. Prog Neurobiol. 2013;100:1–14.

    PubMed  Google Scholar 

  129. Pennartz CMA, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci. 2004;24(29):6446–56.

    CAS  PubMed  Google Scholar 

  130. Lansink CS, Goltstein PM, Lankelma JV, Joosten RNJMA, McNaughton BL, Pennartz CMA. Preferential reactivation of motivationally relevant information in the ventral striatum. J Neurosci. 2008;28(25):6372–82.

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CMA. Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 2009;7(8):e1000173.

    PubMed Central  PubMed  Google Scholar 

  132. Jones M, Wilson M. Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus. 2005;15:867–73.

    PubMed  Google Scholar 

  133. Jones M, Wilson M. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2004;3:e402.

    Google Scholar 

  134. van der Meer MAA, Redish AD. Theta phase precession in rat ventral striatum links place and reward information. J Neurosci. 2011;31(8):2843–54.

    PubMed Central  PubMed  Google Scholar 

  135. Carr M, Karlsson M, Frank L. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron. 2012;75:700–13.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Andrew E. Papale for helpful discussions and comments on an earlier version of this manuscript. This work was supported by a University of Minnesota Doctoral Dissertation Fellowship (AMW) and R01-MH-080318 (ADR).

Author information

Authors and Affiliations

  1. Graduate Program in Neuroscience, University of Minnesota, 6-145 Jackson Hall, 321 Church St. SE, Minneapolis, MN, 55455, USA

    Andrew M. Wikenheiser

  2. Department of Neuroscience, University of Minnesota, 6-145 Jackson Hall, 321 Church St. SE, Minneapolis, MN, 55455, USA

    A. David Redish Ph.D.

Authors
  1. Andrew M. Wikenheiser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. David Redish Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. David Redish Ph.D. .

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

Wikenheiser, A.M., Redish, A.D. (2015). Hippocampal Sequences and the Cognitive Map. 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_5

Download citation

Publish with us

Policies and ethics

Search

Navigation