Skip to main content

Artificial Neural Networks as Models of Robustness in Development and Regeneration: Stability of Memory During Morphological Remodeling

  • Chapter
  • First Online:
Artificial Neural Network Modelling

Part of the book series: Studies in Computational Intelligence ((SCI,volume 628))

Abstract

Artificial neural networks are both a well-established tool in machine learning and a mathematical model of distributed information processing. Developmental and regenerative biology is in desperate need of conceptual models to explain how some species retain memories despite drastic reorganization, remodeling, or regeneration of the brain. Here, we formalize a method of artificial neural network perturbation and quantitatively analyze memory persistence during different types of topology change. We introduce this system as a computational model of the complex information processing mechanisms that allow memories to persist during significant cellular and morphological turnover in the brain. We found that perturbations in artificial neural networks have a general negative effect on the preservation of memory, but that the removal of neurons with different firing patterns can effectively minimize this memory loss. The training algorithms employed and the difficulty of the pattern recognition problem tested are key factors determining the impact of perturbations. The results show that certain perturbations, such as neuron splitting and scaling, can achieve memory persistence by functional recovery of lost patterning information. The study of models integrating both growth and reduction, combined with distributed information processing is an essential first step for a computational theory of pattern formation, plasticity, and robustness.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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. D. Blackiston, T. Shomrat, M. Levin, The stability of memories during brain remodeling: a perspective, Communicative and Integrative Biology (In Press, 2015)

    Google Scholar 

  2. J.V. McConnell, A.L. Jacobson, D.P. Kimble, The effects of regeneration upon retention of a conditioned response in the planarian. J. Comp. Physiol. Psychol. 52, 1–5 (1959)

    Article  Google Scholar 

  3. D.J. Blackiston, E. Silva Casey, M.R. Weiss, Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar?. PLoS ONE 3, e1736 (2008)

    Google Scholar 

  4. J.M. Mateo, Self-referent phenotype matching and long-term maintenance of kin recognition. Anim. Behav. 80, 929–935 (2010)

    Article  Google Scholar 

  5. K.J. Anil, Artificial neural networks: a tutorial (1996), pp. 31–44, http://doi.ieeecomputersociety.org/10.1109/2.485891

  6. H. White, Artificial Neural Networks: Approximation and Learning Theory (Blackwell Publishers, Inc., 1992)

    Google Scholar 

  7. P. Arlotta, B. Berninger, Brains in metamorphosis: reprogramming cell identity within the central nervous system. Curr. Opin. Neurobiol. 27, 208–214 (2014)

    Article  Google Scholar 

  8. D.A. Berg, L. Belnoue, H. Song, A. Simon, Neurotransmitter-mediated control of neurogenesis in the adult vertebrate brain. Development 140, 2548–2561 (2013)

    Article  Google Scholar 

  9. M. Koehl, D.N. Abrous, A new chapter in the field of memory: adult hippocampal neurogenesis. Eur. J. Neurosci. 33, 1101–1114 (2011)

    Article  Google Scholar 

  10. W. Deng, J.B. Aimone, F.H. Gage, New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339–350 (2010)

    Article  Google Scholar 

  11. Y. Kitabatake, K.A. Sailor, G.L. Ming, H. Song, Adult neurogenesis and hippocampal memory function: new cells, more plasticity, new memories?. Neurosurg. Clin. North Am. 18, 105–13 (2007)

    Google Scholar 

  12. S. Couillard-Despres, B. Iglseder, L. Aigner, Neurogenesis, cellular plasticity and cognition: the impact of stem cells in the adult and aging brain–a mini-review. Gerontology 57, 559–564 (2011)

    Article  Google Scholar 

  13. C. Wiltrout, B. Lang, Y. Yan, R.J. Dempsey, R. Vemuganti, Repairing brain after stroke: A review on post-ischemic neurogenesis. Mech. Neurodegeneration 50, 1028–1041 (2007)

    Google Scholar 

  14. T. Tully, V. Cambiazo, L. Kruse, Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci. 14, 68–74 (1994)

    Google Scholar 

  15. M. Gandolfi, L. Mattiacci, S. Dorn, Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 270, 2623–2629 (2003)

    Article  Google Scholar 

  16. K. Rietdorf, J.L.M. Steidle, Was Hopkins right? Influence of larval and early adult experience on the olfactory response in the granary weevil Sitophilus granarius (Coleoptera, Curculionidae). Physiological Entomol. 27, 223–227 (2002)

    Article  Google Scholar 

  17. K. Agata, Y. Umesono, Brain regeneration from pluripotent stem cells in planarian. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 2071–2078 (2008)

    Article  Google Scholar 

  18. T. Shomrat, M. Levin, An automated training paradigm reveals long-term memory in planarians and its persistence through head regeneration. J. Expe. Biol. 216, 3799–3810 (2013)

    Article  Google Scholar 

  19. R.A. Fricker, M.K. Carpenter, C. Winkler, C. Greco, M.A. Gates, A. Björklund, Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the Adult Rat Brain. J. Neurosci. 19, 5990–6005 (1999)

    Google Scholar 

  20. A. Wennersten, X. Meijer, S. Holmin, L. Wahlberg, T. Mathiesen, Proliferation, migration, and differentiation of human neural stem/progenitor cells after transplantation into a rat model of traumatic brain injury. J. Neurosurg. 100, 88–96 (2004)

    Article  Google Scholar 

  21. K.G. Akers, A. Martinez-Canabal, L. Restivo, A.P. Yiu, A. De Cristofaro, H.-L. Hsiang et al., Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344, 598–602 (2014)

    Article  Google Scholar 

  22. L.J. Martin, Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J. Neuropathol. Exp. Neurol. 58, 459–471 (1999)

    Article  Google Scholar 

  23. W.M. Cowan, J.W. Fawcett, D.D. O’Leary, B.B. Stanfield, Regressive events in neurogenesis. Science 225, 1258–1265 (1984)

    Article  Google Scholar 

  24. Y. Xiong, A. Mahmood, M. Chopp, Angiogenesis, neurogenesis and brain recovery of function following injury. Curr. Opin. Investig. Drugs (Lond., Engl.: 2000) 11, 298–308 (2010)

    Google Scholar 

  25. I.A. Basheer, M. Hajmeer, Artificial neural networks: fundamentals, computing, design, and application. J. Microbiol. Methods 43, 3–31 (2000)

    Google Scholar 

  26. M. Anthony, P.L. Bartlett, Neural Network Learning: Theoretical Foundations (Cambridge University Press, 2009)

    Google Scholar 

  27. S. Haykin, Neural Networks: A Comprehensive Foundation (Prentice Hall PTR, 1998)

    Google Scholar 

  28. A.M. Hermundstad, K.S. Brown, D.S. Bassett, J.M. Carlson, Learning, memory, and the role of neural network architecture. PLoS Comput. Biol. 7, e1002063 (2011)

    Article  MathSciNet  Google Scholar 

  29. P.G. Benardos, G.C. Vosniakos, Optimizing feedforward artificial neural network architecture. Eng. Appl. Artif. Intell. 20, 365–382 (2007)

    Article  Google Scholar 

  30. M.M. Islam, M.A. Sattar, M.F. Amin, K. Murase, A new adaptive strategy for pruning and adding hidden neurons during training artificial neural networks, in Intelligent Data Engineering and Automated Learning—IDEAL 2008, vol. 5326, ed. by C. Fyfe, D. Kim, S.-Y. Lee, H. Yin (Springer Berlin Heidelberg, 2008), pp. 40–48

    Google Scholar 

  31. Y. Lecun, J.S. Denker, S.A. Solla, Optimal Brain Damage, pp. 598–605

    Google Scholar 

  32. K.O. Stanley, R. Miikkulainen, Efficient reinforcement learning through evolving neural network topologies. Network (Phenotype) 1, 3 (1996)

    Google Scholar 

  33. A.N. Hampton, C. Adami, Evolution of robust developmental neural networks. Proc. Artif. Life 9, 438–443 (2004)

    Google Scholar 

  34. J.F. Miller, Evolving developmental programs for adaptation, morphogenesis, and self-repair, in Advances in Artificial Life (Springer, 2003), pp. 256–265

    Google Scholar 

  35. J.C. Astor, C. Adami, A developmental model for the evolution of artificial neural networks. Artif. Life 6, 189–218 (2000)

    Article  Google Scholar 

  36. J.E. Auerbach, J.C. Bongard, Evolving CPPNs to grow three-dimensional physical structures, in Proceedings of the 12th Annual Conference on GENETIC and Evolutionary Computation (2010), pp. 627–634

    Google Scholar 

  37. N. Bessonov, M. Levin, N. Morozova, N. Reinberg, A. Tosenberger, V. Volpert, On a model of pattern regeneration based on cell memory. PLoS ONE 10, e0118091 (2015)

    Article  Google Scholar 

  38. U. Yerushalmi, M. Teicher, Evolving synaptic plasticity with an evolutionary cellular development model. PLoS ONE 3, e3697 (2008)

    Article  Google Scholar 

  39. K.O. Stanley, Compositional pattern producing networks: A novel abstraction of development. Genet. Program Evolvable Mach. 8, 131–162 (2007)

    Article  Google Scholar 

  40. M. a. N. N. T. R., Natick (The MathWorks, Inc., Massachusetts, United States, 2012)

    Google Scholar 

  41. R. Hecht-Nielsen, Theory of the backpropagation neural network, in Neural Networks, 1989. IJCNN., International Joint Conference on, vil. 1 (1989), pp. 593–605

    Google Scholar 

  42. D. Marquardt, An algorithm for least-squares estimation of nonlinear parameters. J. Soc. Ind. Appl. Math. 11, 431–441 (1963)

    Article  MathSciNet  MATH  Google Scholar 

  43. M. Riedmiller, H. Braun, A direct adaptive method for faster backpropagation learning: the RPROP algorithm, in IEEE International Conference on Neural Networks, pp. 586–591

    Google Scholar 

  44. N.J. Oviedo, P.A. Newmark, A. Sánchez Alvarado, Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev. Dyn. 226, 326–333 (2003)

    Google Scholar 

  45. G. Deco, E.T. Rolls, L. Albantakis, R. Romo, Brain mechanisms for perceptual and reward-related decision-making. Prog. Neurobiol. 103, 194–213 (2013)

    Article  Google Scholar 

  46. K.D. Birnbaum, A.S. Alvarado, Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008)

    Article  Google Scholar 

  47. D. Lobo, M. Solano, G.A. Bubenik, M. Levin, A linear-encoding model explains the variability of the target morphology in regeneration. J. R. Soc., Interface/R. Soc. 11, 20130918 (2014)

    Article  Google Scholar 

  48. L.N. Vandenberg, D.S. Adams, M. Levin, Normalized shape and location of perturbed craniofacial structures in the Xenopus tadpole reveal an innate ability to achieve correct morphology. Dev. Dyn. 241, 863–878 (2012)

    Article  Google Scholar 

  49. J. Mustard, M. Levin, Bioelectrical mechanisms for programming growth and form: taming physiological networks for soft body robotics, Soft Rob. 1, 169–191 (2014)

    Google Scholar 

  50. A. Tseng, M. Levin, Cracking the bioelectric code: Probing endogenous ionic controls of pattern formation. Commun. Integr. Biol. 6, 1–8 (2013)

    Article  Google Scholar 

  51. M. Levin, C.G. Stevenson, Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu. Rev. Biomed. Eng. 14, 295–323 (2012)

    Article  Google Scholar 

  52. M. Levin, Molecular bioelectricity: how endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo. Mol. Biol. Cell 25, 3835–3850 (2014)

    Article  Google Scholar 

  53. M. Levin, Reprogramming cells and tissue patterning via bioelectrical pathways: molecular mechanisms and biomedical opportunities. Wiley Interdisc. Rev.: Syst. Biol. Med. 5, 657–676 (2013)

    Google Scholar 

  54. M. Levin, Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. Bio Syst. 109, 243–261 (2012)

    Google Scholar 

  55. M. Levin, Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration. J. Physiol. 592, 2295–2305 (2014)

    Google Scholar 

  56. F. Keijzer, M. van Duijn, P. Lyon, What nervous systems do: early evolution, input-output, and the skin brain thesis. Adapt. Behav. 21, 67–85 (2013)

    Article  Google Scholar 

  57. N.D. Holland, Early central nervous system evolution: an era of skin brains? Nat. Rev. Neurosci. 4, 617–627 (2003)

    Article  Google Scholar 

  58. G.A. Buznikov, Y.B. Shmukler, Possible role of “prenervous” neurotransmitters in cellular interactions of early embryogenesis: a hypothesis. Neurochem. Res. 6, 55–68 (1981)

    Article  Google Scholar 

  59. G. Buznikov, Y. Shmukler, J. Lauder, From oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell. Mol. Neurobiol. 16, 537–559 (1996)

    Article  Google Scholar 

  60. H. Yan, L. Zhao, L. Hu, X. Wang, E. Wang, J. Wang, Nonequilibrium landscape theory of neural networks. Proc. Natl. Acad. Sci. 110, E4185–E4194 (2013)

    Article  Google Scholar 

  61. K. Friston, B. SenGupta, G. Auletta, Cognitive dynamics: From attractors to active inference. Proc. IEEE 102, 427–445 (2014)

    Article  Google Scholar 

  62. S. Bhattacharya, Q. Zhang, M. Andersen, A deterministic map of Waddington’s epigenetic landscape for cell fate specification. BMC Syst. Biol. 5, 85 (2011)

    Article  Google Scholar 

  63. B.D. MacArthur, A. Ma’ayan, I. Lemischka, Toward stem cell systems biology: from molecules to networks and landscapes. Cold Spring Harb. Symp.Quant. Biol. 2008, p. sqb. 2008.73. 061

    Google Scholar 

  64. S. Huang, The molecular and mathematical basis of Waddington’s epigenetic landscape: A framework for post-Darwinian biology? BioEssays 34, 149–157 (2012)

    Article  Google Scholar 

  65. E. Aboukhatwa, A. Aboobaker, An introduction to planarians and their stem cells,” in eLS, ed (John Wiley and Sons, Ltd, 2015)

    Google Scholar 

  66. D. Lobo, W.S. Beane, M. Levin, Modeling planarian regeneration: a primer for reverse-engineering the worm. PLoS Comput. Biol. 8, e1002481 (2012)

    Article  Google Scholar 

  67. E. Saló, K. Agata, Planarian regeneration: a classic topic claiming new attention. Int. J. Dev. Biol. 56, 1–4 (2012)

    Article  Google Scholar 

  68. P.W. Reddien, A. Sanchez Alvarado, Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20, 725–57 (2004)

    Google Scholar 

  69. N.J. Oviedo, J. Morokuma, P. Walentek, I. Kema, M.B. Gu, J.-M. Ahn et al., Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev. Biol. 339, 188–199 (2010)

    Article  Google Scholar 

  70. T. Kohonen, Self-organized formation of topologically correct feature maps. Biol. Cybern. 43, 59–69 (1982)

    Article  MathSciNet  MATH  Google Scholar 

Download references

Acknowledgments

We thank the Levin lab, Francisco J. Vico, and many others in the community for helpful discussions at the intersection of neuroscience and developmental biology. This work was supported by NSF (subaward #CBET-0939511 via EBICS at MIT), the G. Harold and Leila Y. Mathers Charitable, and Templeton World Charity Foundations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Levin .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Hammelman, J., Lobo, D., Levin, M. (2016). Artificial Neural Networks as Models of Robustness in Development and Regeneration: Stability of Memory During Morphological Remodeling. In: Shanmuganathan, S., Samarasinghe, S. (eds) Artificial Neural Network Modelling. Studies in Computational Intelligence, vol 628. Springer, Cham. https://doi.org/10.1007/978-3-319-28495-8_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-28495-8_3

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-28493-4

  • Online ISBN: 978-3-319-28495-8

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics