Global remapping emerges as the mechanism for renewal of context-dependent behavior in a reinforcement learning model.

David Kappel, Sen Cheng
Author Information
  1. David Kappel: Institute for Neural Computation, Faculty of Computer Science, Ruhr University Bochum, Bochum, Germany.
  2. Sen Cheng: Institute for Neural Computation, Faculty of Computer Science, Ruhr University Bochum, Bochum, Germany.

Abstract

Introduction: The hippocampal formation exhibits complex and context-dependent activity patterns and dynamics, e.g., place cell activity during spatial navigation in rodents or remapping of place fields when the animal switches between contexts. Furthermore, rodents show context-dependent renewal of extinguished behavior. However, the link between context-dependent neural codes and context-dependent renewal is not fully understood.
Methods: We use a deep neural network-based reinforcement learning agent to study the learning dynamics that occur during spatial learning and context switching in a simulated ABA extinction and renewal paradigm in a 3D virtual environment.
Results: Despite its simplicity, the network exhibits a number of features typically found in the CA1 and CA3 regions of the hippocampus. A significant proportion of neurons in deeper layers of the network are tuned to a specific spatial position of the agent in the environment-similar to place cells in the hippocampus. These complex spatial representations and dynamics occur spontaneously in the hidden layer of a deep network during learning. These spatial representations exhibit global remapping when the agent is exposed to a new context. The spatial maps are restored when the agent returns to the previous context, accompanied by renewal of the conditioned behavior. Remapping is facilitated by memory replay of experiences during training.
Discussion: Our results show that integrated codes that jointly represent spatial and task-relevant contextual variables are the mechanism underlying renewal in a simulated DQN agent.

Keywords

References

  1. Neural Comput. 2007 Dec;19(12):3173-215 [PMID: 17970649]
  2. Sci Rep. 2023 Dec 15;13(1):22335 [PMID: 38102369]
  3. PLoS Comput Biol. 2013 Apr;9(4):e1003024 [PMID: 23592970]
  4. Neuron. 2020 Apr 22;106(2):291-300.e6 [PMID: 32070475]
  5. Neural Netw. 2005 Nov;18(9):1163-71 [PMID: 16198539]
  6. Front Behav Neurosci. 2018 Jan 04;11:253 [PMID: 29354038]
  7. Nat Rev Neurosci. 2020 Mar;21(3):153-168 [PMID: 32042144]
  8. Hippocampus. 2020 Aug;30(8):851-864 [PMID: 31571314]
  9. Behav Processes. 2017 Feb;135:113-131 [PMID: 28034697]
  10. Nature. 1999 Feb 18;397(6720):613-6 [PMID: 10050854]
  11. Nature. 2011 Sep 28;478(7368):246-9 [PMID: 21964339]
  12. J Neurosci. 1997 Aug 1;17(15):5900-20 [PMID: 9221787]
  13. Science. 2005 Jul 22;309(5734):619-23 [PMID: 16040709]
  14. Sci Rep. 2017 Apr 11;7:46071 [PMID: 28397861]
  15. Prog Neurobiol. 2022 Oct;217:102329 [PMID: 35870678]
  16. Biol Psychiatry. 2013 Feb 15;73(4):345-52 [PMID: 22981655]
  17. Sci Adv. 2018 Oct 24;4(10):eaau3075 [PMID: 30417090]
  18. PLoS Comput Biol. 2013;9(12):e1003383 [PMID: 24348230]
  19. Elife. 2023 Mar 14;12: [PMID: 36916899]
  20. PLoS Comput Biol. 2015 May 08;11(5):e1004250 [PMID: 25954996]
  21. Nat Commun. 2021 Apr 22;12(1):2392 [PMID: 33888694]
  22. Learn Mem. 2005 Mar-Apr;12(2):193-208 [PMID: 15774943]
  23. Front Neuroinform. 2023 Mar 09;17:1134405 [PMID: 36970657]
  24. Nature. 2021 Dec;600(7889):489-493 [PMID: 34819674]
  25. Neuron. 2015 Oct 7;88(1):47-63 [PMID: 26447572]
  26. Neuroimage. 2013 Nov 1;81:131-143 [PMID: 23684875]
  27. Science. 2010 Jun 4;328(5983):1288-90 [PMID: 20522777]
  28. Nature. 2006 Mar 30;440(7084):680-3 [PMID: 16474382]
  29. Nat Neurosci. 2018 Nov;21(11):1609-1617 [PMID: 30349103]
  30. Cell. 2020 Nov 25;183(5):1249-1263.e23 [PMID: 33181068]
  31. Psychol Rev. 2007 Jul;114(3):784-805 [PMID: 17638506]
  32. Elife. 2016 Dec 02;5: [PMID: 27911261]
  33. Nat Neurosci. 2021 May;24(5):705-714 [PMID: 33753945]
  34. Learn Mem. 2004 Sep-Oct;11(5):485-94 [PMID: 15466298]
  35. Nature. 2017 Mar 29;543(7647):719-722 [PMID: 28358077]
  36. Cogn Neurodyn. 2012 Oct;6(5):399-407 [PMID: 24082961]
  37. Neural Plast. 2011;2011:203462 [PMID: 21918724]
  38. Neuron. 2021 Oct 6;109(19):3149-3163.e6 [PMID: 34450026]
  39. PLoS One. 2018 Oct 4;13(10):e0204685 [PMID: 30286147]
  40. Elife. 2017 Mar 15;6: [PMID: 28294944]
  41. J Neurosci. 2009 Aug 5;29(31):9918-29 [PMID: 19657042]
  42. J Neurosci. 2017 Jun 28;37(26):6359-6371 [PMID: 28546308]
  43. Ann Neurosci. 2010 Jul;17(3):136-41 [PMID: 25205891]
  44. PLoS Biol. 2006 May;4(5):e120 [PMID: 16605306]
  45. Science. 2010 Feb 12;327(5967):863-6 [PMID: 20075215]
  46. J Neurosci. 1996 Mar 15;16(6):2112-26 [PMID: 8604055]
  47. Physiol Rev. 2021 Apr 1;101(2):611-681 [PMID: 32970967]
  48. PLoS Comput Biol. 2019 Sep 16;15(9):e1007331 [PMID: 31525176]
  49. Neural Netw. 2022 Jul;151:317-335 [PMID: 35468492]
  50. Anim Cogn. 2021 Nov;24(6):1279-1297 [PMID: 33978856]
  51. J Exp Biol. 1996 Jan;199(Pt 1):173-85 [PMID: 8576689]
  52. Learn Mem. 2004 Sep-Oct;11(5):598-603 [PMID: 15466314]
  53. Elife. 2020 Jun 09;9: [PMID: 32515352]
  54. Sci Rep. 2021 Feb 1;11(1):2713 [PMID: 33526840]
  55. Exp Brain Res. 1978 Apr 14;31(4):573-90 [PMID: 658182]
  56. Cell. 2021 Sep 2;184(18):4640-4650.e10 [PMID: 34348112]
  57. Neuropsychopharmacology. 2014 Aug;39(9):2161-9 [PMID: 24625752]
  58. PLoS Comput Biol. 2022 Oct 31;18(10):e1010320 [PMID: 36315587]
  59. Learn Mem. 2008 Apr 03;15(4):244-51 [PMID: 18391185]

Word Cloud

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