Skip to main content
Log in

A neural model of schemas and memory encoding

  • Original Article
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

The ability to rapidly assimilate new information is essential for survival in a dynamic environment. This requires experiences to be encoded alongside the contextual schemas in which they occur. Tse et al. (Science 316(5821):76–82, 2007) showed that new information matching a preexisting schema is learned rapidly. To better understand the neurobiological mechanisms for creating and maintaining schemas, we constructed a biologically plausible neural network to learn context in a spatial memory task. Our model suggests that this occurs through two processing streams of indexing and representation, in which the medial prefrontal cortex and hippocampus work together to index cortical activity. Additionally, our study shows how neuromodulation contributes to rapid encoding within consistent schemas. The level of abstraction of our model further provides a basis for creating context-dependent memories while preventing catastrophic forgetting in artificial neural networks.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

References

  • Abraham WC, Robins A (2005) Memory retention-the synaptic stability versus plasticity dilemma. Trends Neurosci 28(2):73–78

    Article  CAS  Google Scholar 

  • Aston-Jones G, Cohen JD (2005) Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. J Compar Neurol 493(1):99–110

    Article  CAS  Google Scholar 

  • Atherton LA, Dupret D, Mellor JR (2015) Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci 38(9):560–570

    Article  CAS  Google Scholar 

  • Baxter MG, Chiba AA (1999) Cognitive functions of the basal forebrain. Curr Opin Neurobiol 9(2):178–183

    Article  CAS  Google Scholar 

  • Berridge CW, Foote SL (1991) Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11(10):3135–3145

    Article  CAS  Google Scholar 

  • Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20(11):4320–4324

    Article  CAS  Google Scholar 

  • Detorakis G, Bartley T, Neftci E (2018) Contrastive hebbian learning with random feedback weights. arXiv preprint arXiv:1806.07406

  • Eichenbaum H (2017) Prefrontal-hippocampal interactions in episodic memory. Nat Rev Neurosci 18(9):547

    Article  CAS  Google Scholar 

  • French RM (1999) Catastrophic forgetting in connectionist networks. Trends Cognit Sci 3(4):128–135

    Article  CAS  Google Scholar 

  • Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cognit Sci 3(9):351–359

    Article  CAS  Google Scholar 

  • Hawkins J, Ahmad S, Cui Y (2017) A theory of how columns in the neocortex enable learning the structure of the world. Front Neural Circuits 11:81

    Article  Google Scholar 

  • Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14(12):7347–7356

    Article  CAS  Google Scholar 

  • van Kesteren MT, Fernández G, Norris DG, Hermans EJ (2010) Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci 107(16):7550–7555

    Article  Google Scholar 

  • van Kesteren MT, Ruiter DJ, Fernández G, Henson RN (2012) How schema and novelty augment memory formation. Trends Nneurosci 35(4):211–219

    Article  Google Scholar 

  • Kirkpatrick J, Pascanu R, Rabinowitz N, Veness J, Desjardins G, Rusu AA, Milan K, Quan J, Ramalho T, Grabska-Barwinska A, et al (2017) Overcoming catastrophic forgetting in neural networks. In: Proceedings of the national academy of sciences, p 201611835

  • Krichmar JL (2008) The neuromodulatory system: a framework for survival and adaptive behavior in a challenging world. Adapt Behav 16(6):385–399

    Article  Google Scholar 

  • Kumaran D, Hassabis D, McClelland JL (2016) What learning systems do intelligent agents need? complementary learning systems theory updated. Trends Cognit Sci 20(7):512–534

    Article  Google Scholar 

  • LeCun Y, Bengio Y, Hinton G (2015) Deep learning. Nature 521(7553):436

    Article  CAS  Google Scholar 

  • Masse NY, Grant GD, Freedman DJ (2018) Alleviating catastrophic forgetting using context-dependent gating and synaptic stabilization. arXiv preprint arXiv:1802.01569

  • Mattar MG, Daw ND (2018) Prioritized memory access explains planning and hippocampal replay. Nat Neurosci 21(11):1609

    Article  CAS  Google Scholar 

  • McClelland JL, McNaughton BL, O’Reilly RC (1995) 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 102(3):419

    Article  Google Scholar 

  • Mermillod M, Bugaiska A, Bonin P (2013) The stability-plasticity dilemma: investigating the continuum from catastrophic forgetting to age-limited learning effects. Front Psychol 4:504

    Article  Google Scholar 

  • Movellan JR (1991) Contrastive Hebbian learning in the continuous Hopfield model. In: Connectionist models. Elsevier, pp 10–17

  • Nakano S, Hattori M (2017) Reduction of catastrophic forgetting in multilayer neural networks trained by contrastive Hebbian learning with pseudorehearsal. In: 2017 IEEE 10th International Workshop on computational intelligence and applications (IWCIA). IEEE, pp 91–95

  • Otmakhova N, Duzel E, Deutch AY, Lisman J (2013) The hippocampal-VTA loop: the role of novelty and motivation in controlling the entry of information into long-term memory. In: Intrinsically motivated learning in natural and artificial systems. Springer, pp 235–254

  • Pfeiffer BE, Foster DJ (2013) Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497(7447):74

    Article  CAS  Google Scholar 

  • Preston AR, Eichenbaum H (2013) Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 23(17):R764–R773

    Article  CAS  Google Scholar 

  • Rumelhart DE, Hinton GE, Williams RJ (1986) Learning representations by back-propagating errors. Nature 323(6088):533

    Article  Google Scholar 

  • Smith DM, Mizumori SJ (2006) Hippocampal place cells, context, and episodic memory. Hippocampus 16(9):716–729

    Article  Google Scholar 

  • Soltoggio A, Stanley KO, Risi S (2017) Born to learn: the inspiration, progress, and future of evolved plastic artificial neural networks. arXiv preprint arXiv:1703.10371

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

    Article  CAS  Google Scholar 

  • Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RG (2007) Schemas and memory consolidation. Science 316(5821):76–82

    Article  CAS  Google Scholar 

  • Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, Bito H, Morris RG (2011) Schema-dependent gene activation and memory encoding in neocortex. Science 333(6044):891–895

    Article  CAS  Google Scholar 

  • Wagatsuma A, Okuyama T, Sun C, Smith LM, Abe K, Tonegawa S (2018) Locus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context. Proc Natl Acad Sci 115(2):E310–E316

    Article  CAS  Google Scholar 

  • Walling SG, Brown RA, Milway JS, Earle AG, Harley CW (2011) Selective tuning of hippocampal oscillations by phasic locus coeruleus activation in awake male rats. Hippocampus 21(11):1250–1262

    Article  Google Scholar 

  • Yu A, Dayan P (2005) Uncertainty, neuromodulation, and attention. Neuron 46(4):681–692

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the participants of the 2017 Telluride Neuromorphic Cognition Workshop, especially Xinyun Zou, Brent Komer, Georgios Detorakis, and Scott Koziol, who worked on a preliminary project leading to the creation of this model.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiffany Hwu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Special Issue entitled ‘Complex Spatial Navigation in Animals, Computational Models and Neuro-inspired Robots’.

This material is based upon work supported by the United States Air Force and DARPA under contract no. FA8750-18-C-0103, and other support in part by Toyota Motor North America and HRL Laboratories, LLC. Any opinions, findings and conclusions or recommendations ex-pressed in this material are those of the author(s) and do not necessarily reflect the views of the United States Air Force and DARPA.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 125 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hwu, T., Krichmar, J.L. A neural model of schemas and memory encoding. Biol Cybern 114, 169–186 (2020). https://doi.org/10.1007/s00422-019-00808-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-019-00808-7

Keywords

Navigation