Skip to main content

Reinforcement Learning and Hippocampal Dynamics

  • 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

Recent experimental findings on hippocampal representational dynamics such as route replay and sweeps match intuitive notions from reinforcement learning including transiently representing potential trajectories and reward locations. We explore these intuitions within a formal reinforcement learning framework and examine how these representational dynamics might be integrated with reinforcement learning algorithms. We suggest that hippocampal representational dynamics can be best integrated within a model-based reinforcement learning framework and show how this framework can be used to cultivate specific quantitative predictions for the control processes that direct and utilize hippocampal representations.

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

Access this chapter

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

    Google Scholar 

  2. Buckner RL, Carroll DC. Self-projection and the brain. Trends Cogn Sci. 2007;11:49–57.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  5. Schacter DL, Addis DR, Buckner RL. Remembering the past to imagine the future: the prospective brain. Nat Rev Neurosci. 2007;8:657–61.

    Article  CAS  PubMed  Google Scholar 

  6. Sutton RS, Barto AG. Reinforcement learning: an introduction. Cambridge, MA: MIT Press; 1998.

    Google Scholar 

  7. Zilli EA, Hasselmo ME. Modeling the role of working memory and episodic memory in behavioral tasks. Hippocampus. 2008;18:193–209.

    Article  PubMed Central  PubMed  Google Scholar 

  8. 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;9:2907–18.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. 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 

  12. 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 

  13. 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 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  PubMed  Google Scholar 

  18. O’Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci. 2008;11:209–15.

    Article  PubMed  Google Scholar 

  19. Tatsuno M, Lipa P, McNaughton BL. Methodological considerations on the use of template matching to study long-lasting memory trace replay. J Neurosci. 2006;26:10727–42.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Csicsvari J, O’Neill J, Allen K, Senior T. Place-selective firing contributes to the reverse-order reactivation of ca1 pyramidal cells during sharp waves in open-field exploration. Eur J Neurosci. 2007;26:704–16.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Hirase H, Leinekugel X, Czurko A, Csicsvari J, Buzsaki G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified. Proc Natl Acad Sci U S A. 2001;98:9386–90.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. van der Meer MAA, Johnson A, Schmitzer-Torbert NC, Redish AD. Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron. 2010;67:25–32.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Muenzinger KF. Vicarious trial and error at a point of choice: a general survey of its relation to learning efficiency. J Genet Psychol. 1938;53:75–86.

    Google Scholar 

  31. Tolman EC. The determiners of behavior at a choice point. Psychol Rev. 1938;46:318–36.

    Article  Google Scholar 

  32. Pfeiffer BE, Foster DJ. Hippocampal place-cell sequences depict future paths to remembered goals. Nature. 2013;497:74–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Bellman R. Dynamic programming. Princeton, NJ: Princeton University Press; 1957.

    Google Scholar 

  34. Rescorla RA, Wagner AR. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokesy WF, editors. Classical conditioning II: current research and theory. New York: Appleton Century Crofts; 1972. p. 64–99.

    Google Scholar 

  35. Sutton RS, Barto AG. Toward a modern theory of adaptive networks: expectation and prediction. Psychol Rev. 1981;88:135–70.

    Article  CAS  PubMed  Google Scholar 

  36. Montague PR, Dayan P, Sejnowski TJ. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci. 1996;16:1936–47.

    CAS  PubMed  Google Scholar 

  37. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science. 1997;275:1593–9.

    Article  CAS  PubMed  Google Scholar 

  38. Daw ND, Niv Y, Dayan P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci. 2005;8:1704–11.

    Article  CAS  PubMed  Google Scholar 

  39. Yin HH, Knowlton BJ, Balleine BW. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci. 2004;19:181–9.

    Article  PubMed  Google Scholar 

  40. Foster DJ, Morris RGM, Dayan P. A model of hippocampally dependent navigation using the temporal difference learning rule. Hippocampus. 2000;10:1–6.

    Article  CAS  PubMed  Google Scholar 

  41. Dietterich TG. Hierarchical reinforcement learning with the maxQ value function decomposition. J Artif Intell Res. 2000;13:227–303.

    Google Scholar 

  42. Sutton RS, Precup D, Singh S. Between MDPs and semi-MDPs: a framework for temporal abstraction in reinforcement learning. Artif Intell. 1999;112:181–211.

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  44. Richmond M, Yee B, Pouzet B, Veenman L, Rawlins J, Feldon J, Bannerman D. 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;113:1189–203.

    Article  CAS  PubMed  Google Scholar 

  45. Olton DS, Becker JT, Handelmann GE. Hippocampal function: working memory or cognitive mapping? Physiol Psychol. 1980;8:239–46.

    Article  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  47. Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci. 2012;15:1032–9.

    Article  CAS  PubMed  Google Scholar 

  48. Singer AC, Carr MF, Karlsson MP, Frank LM. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron. 2013;77:1163–73.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Walker JA, Olton DS. Fimbria-fornix lesions impair spatial working memory but not cognitive mapping. Behav Neurosci. 1984;98:226–42.

    Article  CAS  PubMed  Google Scholar 

  50. 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 

  51. 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 

  52. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM. Schemas and memory consolidation. Science. 2007;316:76–82.

    Article  CAS  PubMed  Google Scholar 

  53. Johnson A, Varberg Z, Benhardus J, Maahs A, Schrater P. The hippocampus and exploration: dynamically evolving behavior and neural representations. Front Hum Neurosci. 2012;6:1–17.

    Article  Google Scholar 

  54. Friston K, Schwartenbeck P, FitzGerald T, Moutoussis M, Behrens T, Dolan RJ. The anatomy of choice: active inference and agency. Front Hum Neurosci. 2013;7:1–18.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adam Johnson Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Johnson, A., Venditto, S. (2015). Reinforcement Learning and Hippocampal Dynamics. 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_14

Download citation

Publish with us

Policies and ethics