Skip to main content
Log in

The influence of computational traits on the natural selection of the nervous system

  • Published:
Natural Computing Aims and scope Submit manuscript

Abstract

This article addresses why the neural network model has been selected by nature against other computational models to generate behavior in complex multicellular clades. This question, which has not yet been addressed in research, should not be ignored because understanding this issue is necessary to have a complete picture of the evolutionary process of the nervous system. The starting point to discuss the issue is a proposal made 30 years ago: the free-moving hypothesis. This proposal establishes prediction as the main function of the brain and that all multicellular organisms that move require a brain in order to make predictions. This article contains a review contrasting this hypothesis with the discoveries made in the last 30 years within different biological kingdoms. Although none of these discoveries contradict the free-moving hypothesis, it still does not answer the main question. Alternative hypotheses about the origin of the nervous system are discussed in this paper, but they also are not able to answer the question. Six hypotheses are proposed as possible answers, and each of them is discussed by comparing neural processing systems with three other alternative processing systems. The result is that the neural processing system is selected against other kinds of processing systems because it has computational robustness to damage, allowing its function of prediction to be more durable. While this result, called the first neural processing principle, answers the initial question and permits a finished proof of the free-moving hypothesis, it gives rise to the question of how computationally robust a system must be to be selected by nature. This paper claims that the system selected must be computationally robust enough to have enough offspring to allow variation. This answer, named the second neural principle, determines the minimum amount of neurons that a neural processing system must have, but not the maximum. To address this issue, the third and fourth neural processing principles are stated, which determine that the maximum number of neurons is limited by energetic restrictions and body size, respectively. The results presented in this paper show that computational robustness is an important parameter to understand the evolution of nervous system.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Notes

  1. Astrocytes also play an important role in the functions of neurons.

  2. Neural network models that overcome the Church-Turing limit are not considered because there is no experimental evidence that this happens in nature (Siegelmann 1998).

References

  • Acar M, Mettetal J, van Oudenaarden A (2008) Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40(4):471–475

    Article  Google Scholar 

  • Agerwala T (1974) Communication with automata. Hopkins computer research report. John Hopkins University, Baltimore

    Google Scholar 

  • Alstott J et al (2009) Modeling the impact of lesions in the human brain. PLoS Comput Biol 5(6):e1000,408

    Article  Google Scholar 

  • Ames-III A (2000) CNS energy metabolism as related to function. Brain Res Rev 34(12):42–68

    Article  Google Scholar 

  • Armitage J, Holland I, Jenal U, Kenny B (2005) Neural networks in bacteria: making connections. J Bacteriol 187(1):26–36

    Article  Google Scholar 

  • Avlund M, Dodd IB, Semsey S, Sneppen K, Krishna S (2009) Why do phage play dice? J Virol 83(22):11416–11420

    Article  Google Scholar 

  • Balaban N et al (2004) Bacterial persistence as a phenotypic switch. Science 305(5690):1622–1625

    Article  Google Scholar 

  • Baluka F et al (2009) The root-brain hypothesis of charles and francis darwin. Plant Signal Behav 4(12):1121–1127

    Article  Google Scholar 

  • Baluska F, Mancuso S (2013) Root apex transition zone as oscillatory zone. Front Plant Sci 4:354

    Article  Google Scholar 

  • Baluska F et al (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends Plant Sci 10(3):106–111

    Article  Google Scholar 

  • Baluska F et al (2008) Vesicular secretion of auxin. Plant Signal Behav 3(4):254–256

    Article  Google Scholar 

  • Bear MF, Connors BW, Paradiso MA (2007) Neuroscience: exploring the brain. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Bejan A (2006) Advanced engineering thermodynamics, 3rd edn. Wiley, Hoboken

    Google Scholar 

  • Bejan A, Lorente S (2011) The constructal law and the evolution of design in nature. Phys Life Rev 8(3):209–240

    Article  Google Scholar 

  • Bellingham MC, Lim R, Walmsley B (1998) Developmental changes in epsc quantal size and quantal content at a central glutamatergic synapse in rat. J Physiol 511(3):861–869

    Article  Google Scholar 

  • Bertens L et al (2015) Modeling biological gradient formation: combining partial differential equations and petri nets. Nat Comput 15(4):665–675

    Article  MathSciNet  Google Scholar 

  • Bindschaedler C et al (2011) Growing up with bilateral hippocampal atrophy: from childhood to teenage. Cortex 47(8):931–944

    Article  Google Scholar 

  • Boisseau RP, Vogel D, Dussutour A (2016) Habituation in non-neural organisms: evidence from slime moulds. In: Proceedings of the royal society of London B: biological sciences, 283(1829)

  • Bond C (2013) Locomotion and contraction in an asconoid calcareous sponge. Invertebr Biol 132(4):283–290

    Article  MathSciNet  Google Scholar 

  • Bouché N, Fromm H (2004) Gaba in plants: just a metabolite? Trends Plant Sci 9(3):110–115

    Article  Google Scholar 

  • Bradford MJ, Roff DA (1993) Bet hedging and the diapause strategies of the cricket Allonemobius fasciatus. Ecology 74(4):1129–1135

    Article  Google Scholar 

  • Branco T, Staras K (2009) The probability of neurotransmitter release: variability and feedback control at single synapses. Nat Rev Neurosci 10:373–383

    Article  Google Scholar 

  • Bray D (2003) Molecular networks: the top-down view. Science 301(5641):1864–1865

    Article  Google Scholar 

  • Brenner E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11(8):413419

    Article  Google Scholar 

  • Brodal P (2010) The central nervous system. Oxford University Press, Oxford

    Google Scholar 

  • Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 12:336–349

    Article  Google Scholar 

  • Butterfield NJ (2015) The neoproterozoic. Curr Biol 25(19):R859–R863

    Article  Google Scholar 

  • Cardelli L, Zavattaro G (2008) On the computational power of biochemistry. In: Horimoto K, Regensburger G, Rosenkranz M, Yoshida H (eds) Algebraic biology, vol 5147. Springer, Berlin, pp 65–80

    Chapter  Google Scholar 

  • Cartwright P et al (2007) Exceptionally preserved jellyfishes from the middle cambrian. PLoS ONE 2(10):e1121

    Article  Google Scholar 

  • Chase R (2000) Structure and function in the cerebral ganglion. Microsc Res Tech 49(6):511–520

    Article  Google Scholar 

  • Cherniak C (1994) Component placement optimization in the brain. J Neurosci 14(4):2418–2427

    Article  Google Scholar 

  • de Mairan J (1729) Observation botanique. Histoire de l’Academie royale des sciences, pp 35–36

  • Delcomyn F (1999) Foundations of neurobiology. WH Freeman, New York

    Google Scholar 

  • Fernando C et al (2009) Molecular circuits for associative learning in single-celled organisms. J R Soc Interface 6(34):463–469

    Article  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30(3):249–257

    Article  Google Scholar 

  • Fukuda M, Yamamoto T, Llins R (2001) The isochronic band hypothesis and climbing fibre regulation of motricity: an experimental study. Eur J Neurosci 13(2):315–326

    Article  Google Scholar 

  • Garm A, Ekstrm P, Boudes M, Nilsson DE (2006) Rhopalia are integrated parts of the central nervous system in box jellyfish. Cell Tissue Res 325(2):333–343

    Article  Google Scholar 

  • Ghosh A, Pal N, Pal S (1995) Modeling of component failure in neural networks for robustness evaluation: an application to object extraction. IEEE Trans Neural Netw 6(3):648–656

    Article  Google Scholar 

  • Glover J, Fritzsch B (2009) Encyclopedia of neuroscience, chap. Brains of primitive chordates. Springer, Berlin

    Google Scholar 

  • Green RM et al (2002) Circadian rhythms confer a higher level of fitness to arabidopsis plants. Plant Physiol 129(2):576–584

    Article  MathSciNet  Google Scholar 

  • Grunfest H (1959) Evolution of nervous control from primitive organisms to man. chap. Evolution of conduction in the nervous system, pp 43–86

  • Hanken J, Wake DB (1993) Miniaturization of body size: organismal consequences and evolutionary significance. Annu Rev Ecol Syst 24:501–519

    Article  Google Scholar 

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60(1):357–377

    Article  Google Scholar 

  • Hedrich R, Salvador-Recatalá V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends Plant Sci 21(5):376–387

    Article  Google Scholar 

  • Hennessey TM, Rucker WB, McDiarmid CG (1979) Classical conditioning in paramecia. Anim Learn Behav 7(4):417–423

    Article  Google Scholar 

  • Hjelmfelt A, Weinberger ED, Ross J (1991) Chemical implementation of neural networks and turing machines. Proc Natl Acad Sci 88(24):10983–10987

    Article  MATH  Google Scholar 

  • Hofman MA (1983) Energy metabolism, brain size and longevity in mammals. Q Rev Biol 58(4):495–512

    Article  Google Scholar 

  • Holland ND (2003) Early central nervous system evolution: an era of skin brains? Nat Rev Neurosci 4(8):617–627

    Article  Google Scholar 

  • Huxley J (2010) Evolution: the modern synthesis. The definitve edition. MIT Press, Cambridge

    Google Scholar 

  • Ionescu M, Păun G, Yokomori T (2006) Spiking neural p systems. Fundam Inf 71(2,3):279–308

    MathSciNet  MATH  Google Scholar 

  • Kalampokis A et al (2003) Robustness in biological neural networks. Phys A 317(34):581–590

    Article  MATH  Google Scholar 

  • Katzenberger RJ et al (2013) A drosophila model of closed head traumatic brain injury. Proc Natl Acad Sci 110(44):E4152–E4159

    Article  Google Scholar 

  • Kazantsev VB et al (2004) Self-referential phase reset based on inferior olive oscillator dynamics. Proc Natl Acad Sci 101(52):18183–18188

    Article  Google Scholar 

  • Keijzer F, van Duijn M, Lyon P (2013) What nervous systems do: early evolution, inputoutput, and the skin brain thesis. Adapt Behav 21(2):67–85

    Article  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (gaba) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509

    Article  Google Scholar 

  • Knoll A (2011) The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39:217–239

    Article  Google Scholar 

  • Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338–341

    Article  Google Scholar 

  • Laughlin SB, Sejnowski TJ (2003) Communication in neural networks. Science 301(5641):18701874

    Article  Google Scholar 

  • Lenton TM et al (2014) Co-evolution of eukaryotes and ocean oxygenation in the neoproterozoic era. Nat Geosci 7:257–265

    Article  Google Scholar 

  • Levy WB, Baxter RA (2002) Energy-efficient neuronal computation via quantal synaptic failures. J Neurosci 22(11):4746–4755

    Article  Google Scholar 

  • Leys S, Mackie G (1997) Electrical recording from a glass sponge. Nature 387:29–30

    Article  Google Scholar 

  • Leys SP (2015) Elements of a ‘nervous system’ in sponges. J Exp Biol 218(4):581–591

    Article  Google Scholar 

  • Llinás R (1987) Mindwaves. chap. “Mindness” as a functional state of the brain. Oxford, pp 339–358

  • Llinás R (2001) I of the vortex: from neurons to self. MIT press, Cambridge

    Google Scholar 

  • Lm A (1994) Molecular computation of solutions to combinatorial problems. Science 266(5187):1021–1024

    Article  Google Scholar 

  • Lyon P (2013) Developing scaffolds in evoution, culture and cognition. chap. Stress in mind: a stress response hypothesis cognitive cognition. MIT Press, pp 171–190

  • Mackie G (2004) Central neural circuitry in the jellyfish Aglantha. Neurosignals 13(1–2):5–19

    Article  Google Scholar 

  • Mackie GO (1970) Neuroid conduction and the evolution of conducting tissues. The quarterly review of biology 45(4):319–332

    Article  Google Scholar 

  • Magnasco MO (1997) Chemical kinetics is turing universal. Phys Rev Lett 78(6):1190–1193

    Article  Google Scholar 

  • Makarenko V, Llins R (1998) Experimentally determined chaotic phase synchronization in a neuronal system. Proc Natl Acad Sci 95(26):15747–15752

    Article  Google Scholar 

  • Masi E et al (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci 106(10):4048–4053

    Article  Google Scholar 

  • Mayr E (1997) The objects of selection. Proc Natl Acad Sci 94(6):2091–2094

    Article  Google Scholar 

  • McClung CR (2006) Plant circadian rhythms. Plant Cell 18(4):792–803

    Article  Google Scholar 

  • McCulloch W, Pitts W (1943) A logical calculus of the ideas immanent in nervous activity. Bull Math Biophys 5:115–133

    Article  MathSciNet  MATH  Google Scholar 

  • Miguel-Tomé S (2015) Trajectories-state: A new neural mechanism to interpretate cerebral dynamics. In: Artificial computation in biology and medicine, Lecture notes in computer science, vol 9107. Springer International Publishing, pp 88–97

  • Mitchell A et al (2009) Adaptive prediction of environmental changes by microorganisms. Nature 460:220–224

    Article  Google Scholar 

  • Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8:845–856

    Article  Google Scholar 

  • Monk T (2014) The evolutionary origin of nervous systems and implications for neural computation. Ph.D. thesis, University of Otago

  • Monk T, Paulin MG (2014) Predation and the origin of neurones. Brain Behav Evol 84:246–261

    Article  Google Scholar 

  • Monk T, Paulin MG, Green P (2015) Ecological constraints on the origin of neurones. J Math Biol 71(6):1299–1324

    Article  MathSciNet  MATH  Google Scholar 

  • Moreno H et al (2009) Synaptic transmission block by presynaptic injection of oligomeric amyloid beta. Proc Natl Acad Sci 106(14):5901–5906

    Article  Google Scholar 

  • Moroz L (2009) On the independent origins of complex brains and neurons. Brain Behav Evol 74:177–190

    Article  Google Scholar 

  • Moroz LL, Kohn AB (2015) Unbiased view of synaptic and neuronal gene complement in ctenophores: are there pan-neuronal and pan-synaptic genes across metazoa? Integr Comp Biol 55(6):1028–1049

    Google Scholar 

  • Moroz L, Kohn A (2016) Independent origins of neurons and synapses: insights from ctenophores. In: Philosophical transactions of the royal society of London B: biological sciences 371(1685):1–14

    Article  Google Scholar 

  • Navlakha S, Barth A, Bar-Joseph Z (2015) Decreasing-rate pruning optimizes the construction of efficient and robust distributed networks. PLoS Comput Biol 11(7):1–23

    Article  Google Scholar 

  • Nickel M (2010) Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless porifera? Invertebr Biol 129(1):1–16

    Article  MathSciNet  Google Scholar 

  • Nickel M et al (2011) The contractile sponge epithelium sensu lato–body contraction of the demosponge tethya wilhelma is mediated by the pinacoderm. J Exp Biol 214(10):1692–1698

    Article  Google Scholar 

  • Niklas KJ, Newman SA (2013) The origins of multicellular organisms. Evol Dev 15(1):41–52

    Article  Google Scholar 

  • Nilsson DE, Gisln L, Coates MM, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201–205

    Article  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211(11):1792–1804

    Article  Google Scholar 

  • Okubo F, Yokomori T (2016) The computational capability of chemical reaction automata. Nat Comput 15(2):215–224

    Article  MathSciNet  MATH  Google Scholar 

  • Oliveira AG et al (2015) Circadian control sheds light on fungal bioluminescence. Curr Biol 25(7):964–968

    Article  Google Scholar 

  • Oyarce P, Gurovich L (2011) Evidence for the transmission of information through electric potentials in injured avocado trees. J Plant Physiol 168(2):103–108

    Article  Google Scholar 

  • Pantin C (1956) The origin of the nervous system. Publicazioni della Stazione Zoologica di Napoli 28:171–181

    Google Scholar 

  • Parker G (1919) Primitive nervous systems. Lippincott, New York

    Google Scholar 

  • Passano LM (1963) Primitive nervous systems. PNAS 50(2):306–313

    Article  Google Scholar 

  • Paulsen O, Heggelund P (1996) Quantal properties of spontaneous epscs in neurones of the guinea-pig dorsal lateral geniculate nucleus. J Physiol 496(3):759–772

    Article  Google Scholar 

  • Păun G (2002) Membrane computing: an introduction. Springer, Berlin

    Book  MATH  Google Scholar 

  • Petri CA (1966) Communication with automata. Tech. Rep. RADC-TR-65–377. Griffiss Air Force Base, New York

  • Polilov A (2008) Anatomy of the smallest of the coleoptera, feather-winged beetles from tribe nanosellini (coleoptera, ptiliidae) and limits to insect miniaturization. Entomol Rev 88:2633

    Article  Google Scholar 

  • Polilov AA (2012) The smallest insects evolve anucleate neurons. Arthropod Struct Dev 41(1):29–34

    Google Scholar 

  • Qian L, Soloveichik D, Winfree E (2011) Efficient turing-universal computation with DNA polymers. In: DNA computing and molecular programming, vol 6518. Springer International Publishing, pp 123–140

  • Ramesh SA et al (2015) Gaba signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6(7879):1–9

    Google Scholar 

  • Renard E et al (2009) Origin of the neuro-sensory system: new and expected insights from sponges. Integr Zool 4(3):294–308

    Article  MathSciNet  Google Scholar 

  • Roberts A (2007) Plasmodesmal Structure and Development. Plasmodesmata, pp. 1–32

  • Rosenblatt F (1958) The perceptron: a probabilistic model for information storage and organization in the brain. Psychol Rev 65(6):386–408

    Article  Google Scholar 

  • Satterlie R (2002) Control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669

    Article  Google Scholar 

  • Satterlie RA (2011) Do jellyfish have central nervous systems? J Exp Biol 214(8):1215–1223

    Article  Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling: why is animal size so important?. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Scialdone A, Howard M (2015) How plants manage food reserves at night: quantitative models and open questions. Front Plant Sci 6(204):1–7

    Google Scholar 

  • Scialdone A et al (2013) Arabidopsis plants perform arithmetic division to prevent starvation at night. Elife 2:e00669. doi:10.7554/eLife.00669

    Article  Google Scholar 

  • Sibaoka T (1991) Rapid plant movements triggered by action potentials. Bot Mag 104(1):73–95

    Article  Google Scholar 

  • Siegelmann HT (1998) Neural networks and analog computation: beyond the turing limit (progress in theoretical computer science). Birkhäuser, Boston

    Google Scholar 

  • Smith C, Pivovarova N, Reese T (2015) Coordinated feeding behavior in trichoplax, an animal without synapses. PLoS ONE 10(9):e0136,098

    Article  Google Scholar 

  • Smith C et al (2014) Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan trichoplax adhaerens. Curr Biol 24(14):1565–1572

    Article  Google Scholar 

  • Soloveichik D, Seelig G, Winfree E (2010) DNA as a universal substrate for chemical kinetics. Proc Natl Acad Sci 107(12):5393–5398

    Article  Google Scholar 

  • Sukhov V, Nerush V, Orlova L, Vodeneev V (2011) Simulation of action potential propagation in plants. J Theor Biol 291:47–55

    Article  MATH  Google Scholar 

  • Tagkopoulos I, Liu YC, Tavazoie S (2008) Predictive behavior within microbial genetic networks. Science 320:1313–1317

    Article  Google Scholar 

  • Thome C et al (2014) Axon-carrying dendrites convey privileged synaptic input in hippocampal neurons. Neuron 83(6):1418–1430

    Article  Google Scholar 

  • Volkov A, Foster J, Markin V (2010) Signal transduction in mimosa pudica: biologically closed electrical circuits. Plant Cell Environ 33(5):816–827

    Google Scholar 

  • Volkov AG, Markin VS (2015) Active and passive electrical signaling in plants. Prog Bot 76:143–176

    Google Scholar 

  • Wall J, Xu J, Wang X (2002) Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res Rev 39(23):181–215

    Article  Google Scholar 

  • Wehner R (2005) Sensory physiology: brainless eyes. Nature 435(7039):157–159

    Article  Google Scholar 

  • Yan X et al (2009) Research progress on electrical signals in higher plants. Prog Nat Sci 19(5):531–541

    Article  Google Scholar 

  • Yang R, Lenaghan SC, Zhang M, Xia L (2010) A mathematical model on the closing and opening mechanism for venus flytrap. Plant Signal Behav 5(8):968–978

    Article  Google Scholar 

  • Yokawa K et al (2014) Binary decisions in maize root behavior: Y-maze system as tool for unconventional computation in plants. Plant Signal Behav 10(5–6):381–390

    Google Scholar 

  • Zhao D et al (2015) High-resolution non-contact measurement of the electrical activity of plants in situ using optical recording. Sci Rep 5:13,425

    Article  Google Scholar 

  • Zylberberg A et al (2011) The human turing machine: a neural framework for mental programs. Trends Cognit Sci 15(7):293–300

    Google Scholar 

Download references

Acknowledgements

Sergio Miguel-Tomé would like to thank Dr. Rodolfo Llinás for conversations that served as the origin of this paper and for encouraging me to write this article. He would also like to acknowledge to Dr. Ángel Porteros, Dr. Luis Alonso Romero and Lori-Ann Tuscan who proofread the paper and gave me suggestions for improvement. Finally, he would like to thank anonymous referees for their comments on this paper

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sergio Miguel-Tomé.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miguel-Tomé, S. The influence of computational traits on the natural selection of the nervous system. Nat Comput 17, 403–425 (2018). https://doi.org/10.1007/s11047-017-9619-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11047-017-9619-0

Keywords

Navigation