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Cited by 171Marine Invertebrate Physiology and EcologyPhilosophy and History of ScienceDevelopmental Biology and Gene Regulation

An option space for early neural evolution

Open access
Jékely, Gáspár, Keijzer, Fred, Godfrey-Smith, Peter·2015·Philosophical Transactions of the Royal Society B: Biological Sciences
DOI 10.1098/rstb.2015.0181PMC PMC4650133

Published version of a preprint

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Abstract

The origin of nervous systems has traditionally been discussed within two conceptual frameworks. Input–output models stress the sensory-motor aspects of nervous systems, while internal coordination models emphasize the role of nervous systems in coordinating multicellular activity, especially muscle-based motility. Here we consider both frameworks and apply them to describe aspects of each of three main groups of phenomena that nervous systems control: behaviour, physiology and development. We argue that both frameworks and all three aspects of nervous system function need to be considered for a comprehensive discussion of nervous system origins. This broad mapping of the option space enables an overview of the many influences and constraints that may have played a role in the evolution of the first nervous systems.

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Claims the paper makes

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  • Findingcitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    In Platynereis larvae, simultaneous arrest of all cilia is triggered by one giant ciliomotor neuron.

    “In Platynereis larvae, the simultaneous arrest of all cilia is triggered by one giant ciliomotor neuron (C. Veraszto ´ and G. Je ´ keley 2015, unpublished data).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites (C. Veraszto ´ and G. Je ´ keley 2015, unpublished data)

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  • Interpretationnone given
    § (b) Internal coordination and input-output systems for muscle-based behaviours · p. 5

    Muscle-based effector systems require complex internal coordination to initiate and control events spread across large multicellular structures.

    “Muscle-based effector systems require quite complex internal coordination to initiate and control events spread out across large multicellular structures.”
    Quote in the paperNot a substantial claim
  • Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    Coordination of cilia can often be achieved by non-neural means, such as hydrodynamic coupling causing metachronal waves.

    “However, coordination of cilia can often be achieved by non-neural means. In particular, adjacent cilia in multiciliated epithelia spontaneously synchronize their beating activity by means of hydrodynamic coupling, leading to the formation of metachronal waves in multiciliated epithelia or ciliary bands [14-16].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [14] 14. Tamm SL. 1984 Mechanical synchronization of ciliary beating within comb plates of ctenophores. J. Exp. Biol. 113 , 401-408. source

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    • cites [15] 15. Guirao B, Joanny J-F. 2007 Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia. Biophys. J. 92 , 1900-1917. (doi:10. 1529/biophysj.106.084897) source

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    • cites [16] 16. Brumley DR, Polin M, Pedley TJ, Goldstein RE. 2012 Hydrodynamic synchronization and metachronal waves on the surface of the colonial alga Volvox carteri . Phys. Rev. Lett. 109 , 268102. (doi:10.1103/ PhysRevLett.109.268102) source

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  • Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    In bilaterians, steering and modification of ciliary motion comes under nervous control.

    “In other cases, however, especially in bilaterians, the steering and modification of ciliary motion does come under nervous control.”
    Quote in the paperNot a substantial claim
  • Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    Ciliary bands can be controlled directly by multifunctional sensory-motor cells, as during phototaxis in Platynereis dumerilii larvae.

    “Ciliary bands can be controlled directly by multifunctional sensory-motor cells, as during phototaxis in the larvae of the annelid Platynereis dumerilii (figure 2) [25].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] 25. Je ´kely G, Colombelli J, Hausen H, Guy K, Stelzer EHK, Ne ´de ´lec F, Arendt D. 2008 Mechanism of phototaxis in marine zooplankton. Nature 456 , 395-399. (doi:10.1038/nature07590) source

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  • Classified as probably not a substantial claim. 37
  • May combine two claims. 34

  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    The presence of a nervous system increases the efficiency of ciliary control because a few sensors can control many effectors.

    “It has been proposed that the presence of a nervous system increases the efficiency of the control of cilia as a few sensors can control many effectors [6] (see also [4]).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [6] 6. Je ´kely G. 2011 Origin and early evolution of neural circuits for the control of ciliary locomotion. Proc. R. Soc. B 278 , 914-922. (doi:10.1098/rspb.2010.2027) source

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    • cites [4] 4. Mackie G. 1970 Neuroid conduction and evolution of conducting tissues. Q. Rev. Biol. 45 , 319-332. (doi:10.1086/406645)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 1. Introduction · p. 3

    Internal coordination models date from the 1950s, especially with Pantin's criticism of Parker for failing to recognize internal coordination in new effector systems, especially muscle.

    “IC models date from the 1950s, especially with the work of Chris Pantin [7], who criticized Parker for failing to recognize the importance of internal coordination in the new effector systems that arose in metazoan evolution, especially with the origin of muscle.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] 7. Pantin C. 1956 The origin of the nervous system. Pubbl. Staz. Zool. Napoli 28 , 171-181.

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  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given
    § 1. Introduction · p. 2

    Achieving organized movement in muscle is a demanding task that should not be taken for granted.

    “Achieving organized movement in a muscle is a demanding task that should not be taken for granted”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation
    § An option space for early neural evolution · p. 2

    The origin of nervous systems has traditionally been discussed within two conceptual frameworks: input-output and internal coordination.

    “The origin of nervous systems has traditionally been discussed within two conceptual frameworks.”
    • Also stated in: § 1. Introduction · p. 2 · plain
      “Historically, the origin of nervous systems has been discussed in the light of two different conceptual models.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [1] 1. Braitenberg V. 1986 Vehicles: experiments in synthetic psychology . Cambridge, MA: MIT Press.

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    • cites [2] 2. Sherrington C. 1906 The integrative action of the nervous system . New Haven, CT: Yale University Press.

      Not checked in the free run.

    • cites [7] 7. Pantin C. 1956 The origin of the nervous system. Pubbl. Staz. Zool. Napoli 28 , 171-181.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning
    § An option space for early neural evolution · p. 2

    Both the input-output and internal coordination frameworks, and all three aspects of nervous system function (behaviour, physiology and development), need to be considered for a comprehensive discussion of nervous system origins.

    “We argue that both frameworks and all three aspects of nervous system function need to be considered for a comprehensive discussion of nervous system origins.”
    • Also stated in: § 1. Introduction · p. 3 · plain
      “Our present aim is to combine the IO and IC models into a single framework; we argue that both need to be considered to understand early neural evolution as they stress different but complementary issues.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The three roles of nervous systems (behaviour, physiology and development) exhaust the main functions that nervous systems control.

  • May combine two claims.

    Premisecitation
    § (c) Internal coordination and input-output systems for gland-based behaviour · p. 6

    Glandular systems are widespread and essential in many animal groups for normal execution of several behaviours, including predation, locomotion and surface adhesion.

    “Such systems are very widespread and are essential in many animal groups for the normal execution of several behaviours, including predation, locomotion and surface adhesion.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [39] 39. Beckmann A et al. 2015 A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge. BMC Biol . 13 , 3. (doi:10.1186/s12915-014-0113-1)

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    • cites [40] 40. Moran Y, Genikhovich G, Gordon D, Wienkoop S, Zenkert C, Ozbek S, Technau U, Gurevitz M. 2012 Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones. Proc. R. Soc. B 279 , 1351-1358. (doi:10.1098/rspb.2011.1731)

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    • cites [41] 41. Franc JM. 1978 Organization and function of ctenophore colloblasts: an ultrastructural study. Biol. Bull. 155 , 527-541. (doi:10.2307/1540788)

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    • cites [42] 42. Haritos VS, Niranjane A, Weisman S, Trueman HE, Sriskantha A, Sutherland TD. 2010 Harnessing disorder: onychophorans use highly unstructured proteins, not silks, for prey capture. Proc. R. Soc. B 277 , 3255-3263. (doi:10.1098/rspb.2010.0604)

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  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Premisenone given
    § 1. Introduction · p. 2

    Many conceptual frameworks used to discuss early neural evolution recognize only a limited subset of the roles nervous systems can play, often sidelining or omitting neural control of development and physiology in favour of behaviour.

    “many of the conceptual frameworks that are used to discuss this work recognize only a limited subset of the range of roles that nervous systems can play; the neural control of development and physiology is often sidelined or omitted in favour of an exclusive focus on behaviour.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning
    § An option space for early neural evolution · p. 2

    Mapping the option space enables an overview of many influences and constraints that may have played a role in the evolution of the first nervous systems.

    “This broad mapping of the option space enables an overview of the many influences and constraints that may have played a role in the evolution of the first nervous systems.”
    • Also stated in: § 1. Introduction · p. 3 · plain
      “This broad mapping of the option space enables a more comprehensive overview of the many influences and constraints that played a role in the evolution of the first nervous systems.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The three roles of nervous systems (behaviour, physiology and development) exhaust the main functions that nervous systems control.
    • Rests on an assumption: The input-output and internal coordination frameworks together cover the relevant conceptual frameworks for early neural evolution.

  • Classified as probably not a substantial claim.

    Premisecitation
    § An option space for early neural evolution · p. 2

    Internal coordination models emphasize the role of nervous systems in coordinating multicellular activity, especially muscle-based motility.

    “internal coordination models emphasize the role of nervous systems in coordinating multicellular activity, especially muscle-based motility”
    • Also stated in: § 1. Introduction · p. 2 · plain
      “IC models hold that a central role of early nervous systems was to induce and coordinate activity internal to large multicellular organizations.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [7] 7. Pantin C. 1956 The origin of the nervous system. Pubbl. Staz. Zool. Napoli 28 , 171-181.

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  • May combine two claims.

    Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    In ciliated larvae, Wnt signalling is the likely ancestral regulator of axial body polarity and planar polarity of cilia.

    “In ciliated larvae, Wnt signalling is the likely ancestral regulator of establishing axial polarity of the body and the planar polarity of cilia.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [18] 18. Momose T, Derelle R, Houliston E. 2008 A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica . - Development 135 , 2105-2113. (doi:10.1242/dev. 021543)

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    • cites [19] 19. Momose T, Kraus Y, Houliston E. 2012 A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development. Development 139 , 4374-4382. (doi:10.1242/dev.084251)

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    • cites [21] 21. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM. 2007 Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2 , e1031. (doi:10. 1371/journal.pone.0001031) source

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    Interpretationreasoning
    § (b) Internal coordination and input-output systems for muscle-based behaviours · p. 5

    Coordination of muscle surfaces is more challenging than ciliated surfaces and does not come for free.

    “While ciliated surfaces require little neural control to act as a coordinated effector, the coordination of muscle surfaces is a more challenging problem-coordination does not come 'for free', as it does in ciliary metachronal waves.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation
    § An option space for early neural evolution · p. 2

    Input-output models stress the sensory-motor aspects of nervous systems.

    “Input-output models stress the sensory-motor aspects of nervous systems”
    • Also stated in: § 1. Introduction · p. 2 · plain
      “According to IO models, the main role of the nervous system is to receive sensory information and process it to produce meaningful motor output.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] 1. Braitenberg V. 1986 Vehicles: experiments in synthetic psychology . Cambridge, MA: MIT Press.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Premisenone given
    § 1. Introduction · p. 3

    An input-output device coordinates what the organism does with the state of the environment, which is act-state coordination.

    “An IO device aims to coordinate what is done by the organism with the state of the environment; it is concerned with act-state coordination”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 1. Introduction · p. 3

    The internal coordination model never became very prominent, although it has recently been reintroduced.

    “While initially taken up by some biologists such as Passano [8] and de Ceccatty [9], the IC model never became very prominent, although recently it has been reintroduced by Keijzer et al. [10].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [8] 8. Passano LM. 1963 Primitive nervous systems. Proc. Natl Acad. Sci. USA 50 , 306-313. (doi:10.1073/ pnas.50.2.306) While the actual historical scenario-or scenarios-for the evolution of the first nervous systems is beyond us for the foreseeable future, we think that the six options that we sketched do provide a general layout of the major constraints that operated on this historical event, or events. Our aim is not to defend one of these options at the expense of another, but to stress their relevance as ways to focus on different neural functions that play complementary roles in understandin

      Not checked in the free run.

    • cites [9] 9. de Ceccatty MP. 1974 The origin of the integrative systems: a change in view derived from research on coelenterates and sponges. Perspect. Biol. Med . 17 , 379-390. (doi:10.1353/pbm.1974.0060)

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    • cites [10] 10. Keijzer F, van Duijn M, Lyon P. 2013 What nervous systems do: early evolution, input-output, and the skin brain thesis. Adapt. Behav. 21 , 67-85. (idoi:10.1177/1059712312465330)

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  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given
    § 1. Introduction · p. 3

    An internal coordination device coordinates different aspects of what an organism does, which is act-act coordination, and coordinates the micro-acts of parts into the macro-acts of a whole.

    “The aim of an IC device, by contrast, is to coordinate different aspects of what an organism does ; it is concerned with act-act coordination.”
    • Also stated in: § 1. Introduction · p. 3 · plain
      “it coordinates the micro-acts of a system's parts into the macro-acts of a whole”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.

    Interpretationnone given
    § 2. What are nervous systems and what do they do? · p. 4

    All three roles of nervous systems (behaviour, physiology and development) probably have considerable evolutionary importance.

    “We will argue that all three roles probably have considerable evolutionary importance.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The three roles of nervous systems (behaviour, physiology and development) exhaust the main functions that nervous systems control.

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given
    § 2. What are nervous systems and what do they do? · p. 4

    The control of development is a fundamental role of all animal nervous systems.

    “The control of development, also neglected in many discussions, is a fundamental role of all animal nervous systems.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 4

    Large-scale non-neural coordination of cilia requires cilia to be properly oriented within the body, which is ensured by planar polarity of cells.

    “The large-scale non-neural coordination of cilia requires that cilia themselves be properly oriented within the body, though. This is ensured by the planar polarity of the cells, which controls the axis of beating [17].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [17] 17. Mitchell B, Stubbs JL, Huisman F, Taborek P, Yu C, Kintner C. 2009 The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr. Biol. 19 , 924-929. (doi:10.1016/j. cub.2009.04.018)

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    Premisenone given
    § 1. Introduction · p. 2

    These frameworks tend to employ an overly simple conception of the role of neural activity in the adaptive shaping of behaviour.

    “In addition, these frameworks tend to employ an overly simple conception of the role of neural activity in the adaptive shaping of behaviour itself.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisenone given
    § 2. What are nervous systems and what do they do? · p. 4

    Nervous systems control three main groups of phenomena: behaviour, physiology and development.

    “Our option space for neural evolution distinguishes three roles that nervous systems play in an organism: the control of behaviour , the control of physiology and the control of development .”
    • Also stated in: § 1. Introduction · p. 3 · plain
      “we apply these two frameworks to describe aspects of each of three main groups of phenomena that nervous systems control: behaviour, physiology and development.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The three roles of nervous systems (behaviour, physiology and development) exhaust the main functions that nervous systems control.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.

    Premisenone given
    § 2. What are nervous systems and what do they do? · p. 3

    The most fundamental features of neural activity are excitability and influencing other cells on small temporal scales (milliseconds to seconds), via synaptic or neuroendocrine means.

    “The most fundamental features of neural activity are excitability, and the influencing of the activity of other cells on small temporal scales (milliseconds to seconds). This can happen either by synaptic (chemical or electrical) or neuroendocrine (paracrine, hormonal) means.”
    Quote in the paperNot a substantial claim

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    Interpretationreasoning
    § (a) Internal coordination and input -output systems for cilia-based behaviours · p. 5

    The addition that neurons make to ciliary systems is on the input-output side; ciliary systems do not require neural control for internal coordination.

    “The addition that neurons make to ciliary systems, then, is on the IO side. Ciliary systems do not require neural control for internal coordination.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 6

    During defaecation in the fly, the hindgut and anal sphincter are driven by sequential activation of motorneurons, representing an internal coordination system, with sensory feedback adding an input-output component.

    “For example, during defaecation behaviour in the fly, the hindgut and anal sphincter are driven by the sequential activation of motorneurons [54], representing an IC system. The motorneurons also receive sensory feedback from a mechanosensory neuron in the anus, adding an IO component to the circuit [54].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] 54. Zhan W, Yan Z, Li B, Jan LY, Jan YN. 2014 Identification of motor neurons and a mechanosensitive sensory neuron in the defecation circuitry of Drosophila larvae. eLife 3 , e03293. (doi:10.7554/eLife.03293)

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    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 7

    Cilia of ependymal cells in vertebrate cerebral ventricle walls are regulated by neuron-derived melanin-concentrating hormone, and adjacent ciliated ependymal cells are electrically coupled, allowing coordination.

    “For example, the cilia of ependymal cells in the wall of the cerebral ventricles in vertebrates are regulated by neuron-derived melanin-concentrating hormone [68].”
    • Also stated in: § 4. Internal coordination and input-output systems for the neural control of physiology · p. 7 · plain
      “Interestingly, as we have seen above for salivary gland cells, the adjacent ciliated ependymal cells are electrically coupled, allowing the coordination of activity (IC aspect) [69].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [68] 68. Conductier G et al. 2013 Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume. Nat. Neurosci. 16 , 845-847. (doi:10.1038/nn.3401)

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    • cites [69] 69. Jarvis CR, Andrew RD. 1988 Correlated electrophysiology and morphology of the ependyma in rat hypothalamus. J. Neurosci. 8 , 3691-3702.

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    Interpretationreasoning
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    Marine larval metamorphosis is triggered by environmental cues and represents an input-output system.

    “Marine larval metamorphosis is triggered by environmental cues and represents an IO system.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Premisenone given
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    Control of development, including metamorphosis, growth, moulting and sexual maturation, is an often-neglected but very important aspect of nervous system function.

    “Another often-neglected but very important aspect of nervous system function is control of development, including metamorphosis, growth, moulting and sexual maturation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § (c) Internal coordination and input-output systems for gland-based behaviour · p. 6

    Ctenophore photocytes are innervated and activated by mechanical stimulation (input-output aspect) but are also electrically coupled, suggesting spread of luminescence excitation among cells (internal coordination aspect).

    “Photocytes are innervated and are activated by mechanical stimulation (IO aspect) [52,53] but they are also electrically coupled, suggesting the spread of luminescence excitation among cells (IC aspect) [53].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [52] 52. Chang JJ. 1954 Analysis of the luminescent response of the ctenophore, Mnemiopsis leidyi , to stimulation. J. Cell Physiol. 44 , 365-394. (doi:10.1002/jcp. 1030440303)

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    • cites [53] 53. Anctil DM. 1985 Ultrastructure of the luminescent system of the ctenophore Mnemiopsis leidyi . Cell Tissue Res. 242 , 333-340. (doi:10.1007/ BF00214545) source

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    Interpretationreasoning
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 6

    These light-tracking input-output functions influence circadian or circalunar clocks, which are intrinsically internal coordination devices and ultimately responsible for periodicity of physiological signals.

    “However, these IO functions influence the circadian or the circalunar clock that are intrinsically IC devices and are ultimately responsible for the periodicity of the physiological signals.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 7

    Homeostatic control requires a mechanism to sense internal states and an effector mechanism to change them (input-output aspect), and has a strong internal coordination character because of negative feedback and regulation of internal conditions.

    “Homeostatic control in general requires a mechanism to sense internal states and an effector mechanism to change them (IO aspect). However, homeostatic control also has a strong IC character, because of the presence of negative feedback and that internal conditions are regulated.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    Other life cycle transitions, such as sexual maturation in vertebrates and ecdysis in insects, are internally coordinated and regulated by complex hormonal or peptidergic signalling.

    “Other life cycle transitions are internally coordinated. Sexual maturation in vertebrates [82], or ecdysis in insects is regulated by complex hormonal or peptidergic signalling.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [82] 82. Messager S et al. 2005 Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl Acad. Sci. USA 102 , 1761-1766. (doi:10.1073/pnas. 0409330102)

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    • cites [83] 83. Kim Y-J, Zitn ˇ an D, Galizia CG, Cho K-H, Adams ME. 2006 A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16 , 1395-1407. (doi:10.1016/j.cub.2006.06.027)

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    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 6

    Melatonin signalling is very old, present in cnidarians and annelids as well as chordates, and can control behavioural changes and aspects of physiology including sleep, appetite and reproduction.

    “Melatonin signalling is very old, seen in cnidarians [59] and annelids [28] as well as chordates [60], and it can control both behavioural changes and several aspects of physiology, including sleep, appetite and reproduction [60,61].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [59] 59. Peres R, Reitzel AM, Passamaneck Y, Afeche S, Cipolla-Neto J, Marques A, Martindale MQ. 2014 Developmental and light-entrained expression of melatonin and its relationship to the circadian clock in the sea anemone Nematostella vectensis . EvoDevo 5 , 26. (doi:10.1186/2041-9139-5-26)

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    • cites [28] 28. Tosches MA, Bucher D, Vopalensky P, Arendt D. 2014 Melatonin signaling controls circadian swimming behavior in marine zooplankton. Cell 159 , 46-57. (doi:10.1016/j.cell.2014.07.042)

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    • cites [60] 60. Gandhi AV, Mosser EA, Oikonomou G, Prober DA. 2015 Melatonin is required for the circadian regulation of sleep. Neuron 85 , 1193-1199. (doi:10.1016/j.neuron.2015.02.016)

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    Premisecitation
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    Developmental changes are often cued by external events (input-output systems), with marine invertebrate larval metamorphosis as the clearest example.

    “Developmental changes are often cued by external events (IO systems). The metamorphosis of marine invertebrate larvae is the clearest example.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    A swimming larva encounters an environmental cue that is processed neurally, and a neuroendocrine cascade then triggers metamorphosis.

    “A swimming larva encounters an environmental cue that is processed neurally [75]. A neuroendocrine cascade then triggers metamorphosis [78].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [75] 75. Hadfield MG, Meleshkevitch EA, Boudko DY. 2000 The apical sensory organ of a gastropod veliger is - a receptor for settlement cues. Biol. Bull. 198 , 67-76. (doi:10.2307/1542804)

      Not checked in the free run.

    • cites [78] 78. Heyland A, Moroz LL. 2006 Signaling mechanisms underlying metamorphic transitions in animals. Integr. Comp. Biol. 46 , 743-759. (doi:10.1093/icb/ icl023)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    In Drosophila, the ecdysis sequence is under control of a peptidergic signalling cascade involving stepwise activation of peptidergic neurons.

    “For example, in Drosophila , the ecdysis sequence is under the control of a peptidergic signalling cascade, involving the stepwise activation of peptidergic neurons [83].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [83] 83. Kim Y-J, Zitn ˇ an D, Galizia CG, Cho K-H, Adams ME. 2006 A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16 , 1395-1407. (doi:10.1016/j.cub.2006.06.027)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 6

    Many marine animals use moonlight to control timing of reproduction; corals spawn once each year controlled by temperature, daily photoperiod and moonlight.

    “Many marine animals make use of moonlight to control the timing of reproduction [62]; corals, for example, spawn once each year in a way controlled by temperature, daily photoperiod and moonlight [63].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [62] 62. Tessmar-Raible K, Raible F, Arboleda E. 2011 Another place, another timer: marine species and the rhythms of life. Bioessays 33 , 165-172. (doi:10.1002/bies.201000096)

      Not checked in the free run.

    • cites [63] 63. Richmond RH, Hunter CL. 1990 Reproduction and recruitment of corals: comparisons among the - Caribbean, the Tropical Pacific, and the Red Sea. Mar. Ecol. Prog. Ser. 60 , 185-203. (doi:10.3354/ meps060185)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § (c) Internal coordination and input-output systems for gland-based behaviour · p. 6

    Several glandular secretion behaviours are under autonomous programmes and represent internal coordination systems, including tube-building by annelids.

    “The above examples were more on the IO side, but several glandular secretion behaviours are under autonomous programmes and represent IC systems, including tube-building by annelids using mucus-producing cells and sand grains [50,51].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [50] 50. Dorsett DA. 1961 The behaviour of Polydora ciliata (Johnst.). Tube-building and burrowing. J. Mar. Biol. Assoc. UK 41 , 577-590. (doi:10.1017/ S0025315400016167)

      Not checked in the free run.

    • cites [51] 51. Ziegelmeier E. 1969 Neue Untersuchungen u ¨ber die Wohnro ¨hren-Bauweise von Lanice conchilega (Polychaeta, Sedentaria). Helgolander Wiss. Meeresunters . 19 , 216-229. (doi:10.1007/ BF01625607)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § (c) Internal coordination and input-output systems for gland-based behaviour · p. 6

    In cnidarians, toxin-gland and cnidocyte discharge are triggered by prey encounter and influenced by light.

    “For example, in cnidarians, toxin-gland and cnidocyte discharge are triggered by prey encounter [40], and are also influenced by light [44] (IO systems).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [40] 40. Moran Y, Genikhovich G, Gordon D, Wienkoop S, Zenkert C, Ozbek S, Technau U, Gurevitz M. 2012 Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones. Proc. R. Soc. B 279 , 1351-1358. (doi:10.1098/rspb.2011.1731)

      Not checked in the free run.

    • cites [44] 44. Plachetzki DC, Fong CR, Oakley TH. 2012 Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol . 10 , 17. (doi:10.1186/ 1741-7007-10-17)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 5. Internal coordination and input-output systems for the neural control of development · p. 7

    Sponge larvae, which lack neurons, also settle and trigger metamorphosis in a roughly similar way, and this transition is potentially significant in the earliest history of nervous systems.

    “Sponge larvae, which do not have neurons, also settle and trigger metamorphosis in a roughly similar way, and this developmental transition in sponges is potentially significant in the earliest history of nervous systems [79].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [79] 79. Degnan SM, Degnan BM. 2010 The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution. Phil. Trans. R. Soc. B 365 , 641-651. (doi:10.1098/rstb.2009.0248)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § (c) Internal coordination and input-output systems for gland-based behaviour · p. 6

    Gland structures such as nematocysts, colloblasts and slime glands are under nervous control, and sensory stimuli regulate secretion or discharge.

    “These structures are under nervous control [41,43] and sensory stimuli regulate secretion or discharge.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [41] 41. Franc JM. 1978 Organization and function of ctenophore colloblasts: an ultrastructural study. Biol. Bull. 155 , 527-541. (doi:10.2307/1540788)

      Not checked in the free run.

    • cites [43] 43. Westfall JA. 1970 The nematocyte complex in a hydromedusan, Gonionemus vertens . Z. Zellforsch. Mik. Ana. 110 , 457-470. (doi:10.1007/ BF00330098)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 7

    Ciliated cells of human airway epithelia express sensory bitter taste receptors, and bitter compounds increase ciliary beat frequency by a cell-autonomous mechanism.

    “Ciliated cells of human airway epithelia express sensory bitter taste receptors, and bitter compounds increase ciliary beat frequency by a cell-autonomous mechanism [71].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [71] 71. Shah A, Ben-Shahar Y, Moninger T, Kline J, Welsh M. 2009 Motile cilia of human airway epithelia are chemosensory. Science 325 , 1131-1134. (doi:10. 1126/science.1173869)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. Internal coordination and input-output systems for the neural control of physiology · p. 6

    Salivary gland cells in gastropod molluscs and mouse are electrically coupled, allowing propagation of action potentials along glandular epithelium and coordinating secretion from many cells; this is an internal coordination system in non-neural excitable cells.

    “Salivary gland cells in gastropod molluscs and the mouse are electrically coupled, which allows the propagation of action potentials along the glandular epithelium, coordinating secretion from many cells [55,56]. This represents an example of an IC system of physiology in non-neural excitable cells.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [55] 55. Kater SB, Galvin NJ. 1978 Physiological and morphological evidence for coupling in mouse salivary gland acinar cells. J. Cell Biol. 79 , 20-26. (doi:10.1083/jcb.79.1.20)

      Not checked in the free run.

    • cites [56] 56. Kater SB, Rued JR, Murphy AD. 1978 Propagation of action potentials through electrotonic junctions in the salivary glands of the pulmonate mollusc, Helisoma trivolvis . J. Exp. Biol. 72 , 77-90.

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    A small motile larva faced input-output problems, whereas a larger adult, perhaps drifting or sessile, faces internal-coordination problems.

    “A small, motile larva faced IO problems; a larger adult, perhaps drifting or sessile, faces IC problems.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning
    § 7. Discussion · p. 8

    Even if a more integrated view is assumed, the IC/IO distinction remains theoretically important because they are two fundamentally different tasks an organism must handle, whether or not they are mechanistically separable.

    “Still, even if this possibility is assumed, we maintain that the distinction between IC and IO functions is theoretically important; these are two fundamentally different tasks that must be handled by an organism, whether they are separable with respect to mechanisms or not.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationnone given
    § 7. Discussion · p. 9

    Researchers in this field tend to adopt one conceptual framework, often an input-output one, and view neural evolution through it.

    “However, we maintain that workers in this field do tend to slip into one conceptual framework or the other-often an IO framework-and see neural evolution through that lens.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 6. Possible historical sequences · p. 8

    Food-related sensory cues may also affect digestive enzyme secretion in Trichoplax.

    “that may also influence digestive enzyme secretion (IO, physiology).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [90] 90. Ueda T, Koya S, Maruyama YK. 1999 Dynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence . Biosystems 54 , 65-70. (doi:10.1016/S0303-2647(99)00066-0)

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    All extant organisms called primitive have a long evolutionary history since the first nervous systems appeared and cannot be treated as representative of a primitive condition without further evidence.

    “The general message remains that all extant 'primitive organisms' have a long evolutionary history since the first nervous systems arose and cannot be without further evidence be taken as representative for any primitive condition.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given
    § 6. Possible historical sequences · p. 8

    All else equal, larger bodies pose greater challenges for internal coordination in behavioural control.

    “Ceteris paribus, larger bodies will present more challenges for internal coordination in the control of behaviour.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    Some of the six options may have become more important than others in different contexts and evolutionary stages.

    “However, in different contexts and at different evolutionary stages, some of our six options may have become more important than others.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    Body size may have played an important role.

    “An important role may be played by body size, for example.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation
    § 6. Possible historical sequences · p. 8

    A control structure for contraction-based motility could have served as a scaffold for later evolution of large-scale external sensors.

    “However, a control structure for contraction-based motility can have acted as a scaffold for the subsequent evolution of large-scale external sensors [88].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [88] 88. Keijzer F. 2015 Moving and sensing without input and output: early nervous systems and the origins of the animal sensorimotor organization. Biol. Philos. 30 , 311-331. (doi:10.1007/s10539015-9483-1) source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning
    § 6. Possible historical sequences · p. 7

    Having a few sensory cells control many motor devices would be more efficient.

    “It would be more efficient for a small number of sensory cells to control a large bank of motor devices”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given
    § References · p. 9

    The actual historical scenario or scenarios for the evolution of the first nervous systems will remain beyond us for the foreseeable future.

    “While the actual historical scenario-or scenarios-for the evolution of the first nervous systems is beyond us for the foreseeable future”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § 7. Discussion · p. 9

    Single-factor explanations are unlikely because precursors of all six nervous-system functions exist in non-neural animals.

    “In particular, single-factor explanations are made unlikely by the existence of precursors in non-neural animals of all six of the functions for nervous systems we have distinguished.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning
    § 7. Discussion · p. 8

    The same may hold for behaviours important in early neural evolution.

    “The same may apply to behaviours that were important in early neural evolution.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 6. Possible historical sequences · p. 8

    In many extant animals, larvae use cilia for movement and later stages use muscle for behaviour; this combination occurs in all animals with a dispersing ciliated larval stage.

    “In many extant animals the larval stage uses cilia for motion while later developmental stages make use of muscle for behaviour-this combination is seen in all animals that have a dispersing ciliated larval stage (e.g. annelids, molluscs, cephalochordates) [92].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [92] 92. Stokes M. 1997 Larval locomotion of the lancelet Branchiostoma floridae . J. Exp. Biol. 200 , 1661-1680.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    Early nervous systems may have had somewhat different roles at different stages of a single organism's life cycle.

    “This raises the possibility, also, that early nervous systems may have played somewhat different roles at different stages in the life cycle of a single organism.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning
    § 6. Possible historical sequences · p. 7

    Neurons enable this more efficient arrangement.

    “and this is what the advent of neurons makes possible.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § 7. Discussion · p. 8

    The swimming-beat contraction of scyphozoan medusae illustrates a default behaviour, and much neural activity in jellyfish maintains this rhythm.

    “The swimming-beat contraction in scyphozoan medusae is a good illustration of a default behaviour in those organisms, and a substantial portion of the neural activity in a jellyfish goes into maintaining this rhythmic behaviour [93,94].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [93] 93. Passano LM. 1965 Pacemakers and activity patterns in medusae: homage to Romanes. Am. Zool. 5 , 465-481. (doi:10.2307/3881171)

      Not checked in the free run.

    • cites [94] 94. Schwab WE. 1977 The ontogeny of swimming behavior in the scyphozoan, Aurelia aurita . I. Electrophysiological analysis. Biol. Bull. 152 , 233-250. (doi:10.2307/1540562)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. Possible historical sequences · p. 7

    A plausible origin account centers on efficient sensory control of locomotion in a ciliated swimming stage of an early metazoan, an input-output behaviour hypothesis.

    “So one plausible account of the origin of nervous systems focuses on the efficient control of locomotion by sensory mechanisms in a ciliated swimming stage of an early metazoan: this is an IO behaviour hypothesis.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationnone given
    § References · p. 9

    The six options provide a general layout of the major constraints that operated on early nervous system evolution.

    “we think that the six options that we sketched do provide a general layout of the major constraints that operated on this historical event, or events.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § 6. Possible historical sequences · p. 8

    Because all six neuronal functions occur in simple form in animals without nervous systems, it is plausible that all six roles evolved in parallel from the beginning.

    “Given that all six of the functions that neurons can play are seen in simple form in animals without nervous systems, it is plausible that all six of the roles we have discussed evolved in parallel from the beginning.”
    Quote in the paperNot a substantial claim
61 of 61

  • The paper relies on this without support.

    Muscle is absent from sponges and placozoa.

    “but is absent from sponges and placozoa.”

  • The paper relies on this without support.

    The three roles of nervous systems (behaviour, physiology and development) exhaust the main functions that nervous systems control.

    “Our option space for neural evolution distinguishes three roles that nervous systems play in an organism: the control of behaviour , the control of physiology and the control of development .”

  • The paper relies on this without support.

    Every organism that possesses a nervous system also has muscle, and the converse holds, with myxozoan cnidarians as the only exceptions.

    “all organisms with nervous systems have muscle, and vice versa .”

  • The paper relies on this without support.

    The input-output and internal coordination frameworks together cover the relevant conceptual frameworks for early neural evolution.

    “The origin of nervous systems has traditionally been discussed within two conceptual frameworks.”

  • The paper relies on this without support.

    Simple marine organisms often undergo dramatic changes between different modes of living and their accompanying morphologies.

    “Simple marine organisms often exhibit dramatic changes between different modes of living and their accompanying morphologies.”

  • The paper relies on this without support.

    Triggering and coordinating metamorphosis in many animals is a crucial life-cycle transition that places significant demands on control systems.

    “The triggering and coordination of metamorphosis for many animals is a crucially important life cycle transition that places significant demands on control systems.”

  • The paper relies on this without support.

    In a sponge larva, non-neural swimming control works by sensory mechanisms influencing cilia on the same cell, steering the whole larva.

    “Here sensory mechanisms influence the activity of cilia on the same cell, thereby steering the whole larva.”

  • The paper relies on this without support.

    Muscle cells and nerve cells, with one exception, always co-occur across animal diversity.

    “muscle cells and nerve cells, bar one exception, always co-occur across animal diversity.”

  • The paper relies on this without support.

    Useful motility requires specific and stereotypical patterns of contraction and extension across the contractile surface.

    “Useful motility requires specific and stereotypical patterns of contraction and extension across this surface.”

  • The paper relies on this without support.

    Sponge metamorphosis is controlled by chemosensing of the substrate, an input-output developmental function.

    “Sponge metamorphosis is controlled by chemosensing of the substrate (IO, development)”

  • The paper relies on this without support.

    Sponge larvae show ciliary locomotion controlled by photoreception, an input-output behavioural function.

    “their larvae exhibit ciliary locomotion controlled by photoreception (IO, behaviour)”

  • The paper relies on this without support.

    Insulin-like peptides and Wamides are ancient molecules with broadly conserved functions.

    “both insulin-like peptides (IC role in physiology and development)andWamides(IOroleintriggeringmetamorphosis) are ancient molecules with broadly conserved functions.”

  • The paper relies on this without support.

    Opsins are old and occur in ctenophores, cnidarians and bilaterians.

    “Opsins (IO roles in behaviour and physiology) are also old, and present in ctenophores, cnidarians and bilaterians.”

  • The authors state this as an assumption.

    The Jékely sequence, with an input-output behaviour function central, assumes a small organism whose behavioural demands for internal coordination are not great.

    “The possible evolutionary sequence due to Je ´kely that was outlined above, in which an IO-behaviour function is central, is based on the assumption of a small organism in which the demands of internal coordination on behaviour are not great.”
14 of 14

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Authors
Jékely, G., Keijzer, F., & Godfrey-Smith, P.
Affiliations
  • Max Planck Institute for Developmental Biology (DE)
  • University of Groningen (NL)
  • Philosophy Program, The Graduate Center, City University of New York, New York, NY 10016, USA
Corresponding author
Jékely, Gáspár
ORCID
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2015-12-19
Volume
370
Issue
1684
Pages
20150181
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2015.0181
PMC
PMC4650133
OpenAlex
W2196464793
Semantic Scholar
1eeb9cab0786130637d54427fdb644d4161c9e42
Cited by
171
References
109
Citations by year
2026: 6 · 2025: 17 · 2024: 27 · 2023: 17 · 2022: 14 · 2021: 24 · 2020: 14 · 2019: 17 · 2018: 11 · 2017: 10 · 2016: 9 · 2015: 5
FWCI
1.47
Type
journal article
Language
en
Open access
Licence
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion, other-oa)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
Funders
  • European Commission (2007–2013, FP7 2007-2013, 260821, FP7/2007)
  • FP7 Ideas: European Research Council (260821)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
neuroevolution, input-output model, sensorimotor control, nervous system function, behavior, development (biology), evolutionary constraints
MeSH terms
Animals, Biological Evolution, Motor Activity, Nervous System, Nervous System Physiological Phenomena

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