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Evolutionary origin of autonomic regulation of physiological activities in vertebrate phyla

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Abstract

Proper regulation of physiological activities is crucial for homeostasis in animals. Autonomic regulation of these activities is most developed in mammals, in which a part of peripheral nervous system, termed the autonomic nervous system plays the dominant role. Circulatory activity and digestive activity in vertebrates change in opposite phases to each other. The stage where circulatory activity is high and digestive activity is low is termed the “fight or flight stage” while the stage where circulatory activity is low and digestive activity is high is termed the “rest and digest stage”. It has been thought that the autonomic nervous system originated in early vertebrate phyla and developed to its greatest extent in mammals. In this study, we compared the pattern of change of circulatory and digestive activities in several invertebrates and found that the two stages seen in mammals are also present in a wide variety of animals, including evolutionarily early-diverging invertebrate taxa. From this and other arguments we propose a novel possibility that the basic properties of the autonomic nervous system were established very early in metazoan evolution.

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Notes

  1. Various types of feeding habit are employed in Mollusks including herbivores (Aplysia), carnivores (Octopus) and scavengers (Babylonia). One thing common to all types is that they use radula for feeding.

  2. In hydra, it is possible to construct animals that have no neurons by treating animals with drugs, e.g. hydroxyurea (HU). HU blocks the transition of cells from G1 to S phase. Virtually, however, a large fraction of cells in S phase are also severely damaged and preferentially eliminated. Since multipotent stem cells in hydra have shorter cell cycle time than epithelial cells, the stem cells that spend larger fraction of time in S phase are more easily damaged and eliminated than epithelial cell lineage. The polyps thus constructed have no neurons leaving secretory gland cells other than epithelial cells. By feeding them by transferring Artemia into the digestive tract by hand, it is possible for the nerve free hydra to survive and moreover even to proliferate by asexual budding.

  3. The myenteric plexus in mammals is made up of multiple ganglia and bundles of neural fibers that connect the ganglia. In contrast, the diffuse nerve net in hydra is made up of single neural cell bodies and single neural fibers that connect the cell bodies. Therefore, the two systems have netlike structure. In the nerve net of hydra, two neuropeptides GLWamide and Hym-355 (FPQSFLPRGamide) are found in the neurons whereas cholinergic neurons and serotonergic neurons are not. Since those two neuropeptides had no effect on digestive movements (T. Fujisawa, personal communication), the hormonal factor that activates digestive movements remains to be discovered.

  4. The measurement was carried out using a wild type strain of Hydra magnipapillata (strain 105) cultured under standard mass culture conditions (Sugiyama and Fujisawa 1977). They were fed three times a week and for each feeding animals were transferred to fresh culture medium 3–5 h after the feeding. An animal that had been starved for 24 h was placed in culture solution in a plastic dish of 50 mm in diameter. Behavior of the animal before and after feeding was recorded with a CCD camera on a dissecting microscope connected to a VCR.

Abbreviations

ANS:

Autonomic nervous system

SNS:

Sympathetic nervous system

PSNS:

Parasympathetic nervous system

CNS:

Central nervous system

ENS:

Enteric nervous system

NE:

Norepinephrine

ACh:

Acetylcholine

5-HT:

5-Hydroxytryptamine

GABA:

4-Aminobutanoic acid

HU:

Hydroxyurea

References

  • Albertson DG, Thomson JU (1976) The pharynx of Caenohabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:299–325

    Article  PubMed  CAS  Google Scholar 

  • Avery L (1993) Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. J Exp Biol 175:283–297

    PubMed  CAS  Google Scholar 

  • Avery L, Horvitz HR (1989) Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of Caenorhabditis elegans. Neuron 3:473–485

    Article  PubMed  CAS  Google Scholar 

  • Bodmer R (1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–729

    PubMed  CAS  Google Scholar 

  • Cannon WB (1929) Bodily Changes in pain, hunger, fear and rage: an account of recent research into the function of emotional excitement, 2nd edn. Appleton-Century-Crofts, New York

    Google Scholar 

  • Cannon WB (1932) The wisdom of the body. Kegan Paul, London

    Google Scholar 

  • Chen JN, Fishman MC (2000) Genetics of heart development. Trends Genet 16:383–388

    Article  PubMed  CAS  Google Scholar 

  • Crick F (1970) Diffusion in embryogenesis. Nature 231:420–422

    Article  Google Scholar 

  • Dieringer N, Koester J, Weiss KR (1978) Adaptive changes in heart rate of Aplysia californica. J Comp Physiol 123:11–21

    Article  Google Scholar 

  • Drushel RF, Neustadter DM, Shallenberger LL, Crago PE, Chiel H.J (1997) The kinematics of swallowing in the buccal mass of Aplysia californica. J Exp Biol 200:735–752

    PubMed  CAS  Google Scholar 

  • Ellis CH (1944) The mechanism of extension in the legs of spiders. Biol Bull 86:41–50

    Article  Google Scholar 

  • Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193

    PubMed  CAS  Google Scholar 

  • Ganong WF (1999) Review of medical physiology. 19th edn. McGraw-Hill Medical Publishing, New York

    Google Scholar 

  • Gershon MD, Erde SM (1981) The nervous system of the gut. Gastroenterology 80:1571–1594

    PubMed  CAS  Google Scholar 

  • Goldstein R, Kistler HB Jr, Steinbusch HWM, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. Neurosci 11:535–547

    Article  CAS  Google Scholar 

  • Grens A, Gee L, Fisher DA, Bode HR (1996) CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. Dev Biol 180:473–488

    Article  PubMed  CAS  Google Scholar 

  • Grens A, Shimizu H, Hoffmeister SA, Bode HR, Fujisawa T (1999) The novel signal peptides, pedibin and Hym-346, lower positional value thereby enhancing foot formation in hydra. Development 126:517–524

    PubMed  CAS  Google Scholar 

  • Hukuhara T, Yamagami M, Nakayama S (1958) On the intestinal intrinsic reflexes. Jpn J Physiol 8:9–20

    PubMed  CAS  Google Scholar 

  • Hukuhara T, Sumi T, Kotani S (1961a) The role of the ganglion cells in the small intestine taken in the intestinal intrinsic reflex. Jpn J Physiol 11:281–288

    PubMed  CAS  Google Scholar 

  • Hukuhara T, Kotani S, Sato G (1961b) Effects of destruction of intramural ganglion cells on colonic motility: possible genesis of congenital megacolon. Jpn J Physiol 11:635–640

    PubMed  CAS  Google Scholar 

  • Kier WM (1988) The arrangement and function of molluscan muscle. In: Trueman ER, Clarke MR (eds), Wilbur KM (Editor-in-Chief) The Mollusca, form and function. Academic, New York, pp 211–252

  • Kier WM, Smith KK (1985) Tongues, tentacles and trunks: The biomechanics of movement in muscular-hydrostats. Zool J Linn Soc 83:307–324

    Google Scholar 

  • Koch UT, Koester J, Weiss KR (1984) Neuronal mediation of cardiovascular effects of food arousal in Aplysia. J Neurophysiol 51:126–135

    PubMed  CAS  Google Scholar 

  • Koester J, Koch UT (1984) Neural control of the circulatory system of Aplysia. Experientia 43:972–980

    Article  Google Scholar 

  • Kupfermann I (1991) Functional studies of cotransmission. Physiol Rev 71:683–732

    PubMed  CAS  Google Scholar 

  • Lenhoff HM (1961) Digestion of ingested protein by Hydra as studied by radioautography and fractionation by differential solubilities. Exp Cell Res 23:335–353

    Article  PubMed  CAS  Google Scholar 

  • Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP (1993) Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:419–431

    PubMed  CAS  Google Scholar 

  • Marcum BA, Campbell RD (1978) Development of Hydra lacking nerve and interstitial cells. J Cell Sci. 29:17–33

    PubMed  CAS  Google Scholar 

  • Matthews GG (1997) Neurobiology: molecules, cells, and systems. Blackwell, New York, pp 23–24

    Google Scholar 

  • Meinhardt H (1997) Models of biological pattern formation. Academic, New York

    Google Scholar 

  • Meinhardt H (2002) The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. Bioessays 24:185–191

    Article  PubMed  Google Scholar 

  • Mitgutsch C, Hauser F, Grimmelikhuijzen CJP (1999) Expression and developmental regulation of the Hydra-RFamide and Hydra-LWamide preprohormone genes in Hydra: evidence for transient phases of head formation. Dev Biol 207:189–203

    Article  PubMed  CAS  Google Scholar 

  • Moosler A, Rinehart KL, Grimmelikhuijzen CJP (1996) Isolation of four novel neuropeptides, the Hydra RFamides I-IV, from Hydra magnipapillata. Biochem Biophys Res Commun 229:596–602

    Article  PubMed  CAS  Google Scholar 

  • Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C, Smeets WJAJ (1998) The central nervous system of vertebrates: an introduction to structure and function. Springer Heidelberg

    Google Scholar 

  • Okkema PG, Ha E, Haun C, Chen W, Fire A (1997) The Caenorhabditis elegans Nk-2 homeobox gene ceh-22 activates pharyngeal muscle gene expression in combination with pha-1 and is required for normal pharyngeal development. Development 124:3965–3973

    PubMed  CAS  Google Scholar 

  • Ono JK, McCaman RE (1984) Immunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia. Neuroscience 11:549–560

    Article  PubMed  CAS  Google Scholar 

  • Parry DA, Brown RHJ (1959) The hydraulic mechanism of the spider leg. J Exp Biol 36:423–433

    Google Scholar 

  • Pennisi E (2003) Drafting a tree. Science 300:1694

    Article  PubMed  Google Scholar 

  • Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671

    Article  PubMed  CAS  Google Scholar 

  • Ram JL, Shukla UA, Ajimal GS (1981) Serotonin has both excitatory and inhibitory modulatory effects on feeding muscle in Aplysia. J Neurobiol 12:613–621

    Article  PubMed  CAS  Google Scholar 

  • Riddle DL, Blumenthal T, Meyer BJ, Priess JR (1997) C. elegans II: monograph 33 (Cold Spring Harbor Monograph Series) Cold Spring Harbor Laboratory Press

  • Robertson D, Low PA, Polinsky RJ (1996) Primer on the autonomic nervous system. Academic, San Diego

    Google Scholar 

  • Ruppert EE, Barnes RD (1996) Invertebrate zoology. Saunders College, Fort Worth

    Google Scholar 

  • Sakaguchi M, Mizusina A, Kobayakawa Y (1996) Structure, development, and maintenance of the nerve net of the body column in Hydra. J Comp Neurol 373:41–54

    Article  PubMed  CAS  Google Scholar 

  • Sarnat HB, Netsky MG (2002) When does a ganglion become a brain? Evolutionary origin of the central nervous system. Semin Pediatr Neurol 9:240–253

    Article  PubMed  Google Scholar 

  • Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619–631

    Article  PubMed  CAS  Google Scholar 

  • Shimizu H, Fujisawa T (2003) Peduncle of Hydra and the heart of higher organisms share a common ancestral origin. genesis 36:182–186

    Article  PubMed  CAS  Google Scholar 

  • Shimizu H, Koizumi O, Fujisawa T (2004) Three digestive movements in Hydra regulated by the diffuse nerve net in the body column. J Comp Physiol A 190:623–630

    Article  Google Scholar 

  • Sugden AM, Jasny BR, Culotta E, Pennisi E (2003) Charting the evolutionary history of life. Science 300:1691

    Article  CAS  Google Scholar 

  • Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in hydra I sexual reproduction of Hydra magnipapillata and isolation of mutants. Dev Growth Differ 19:187–200

    Article  Google Scholar 

  • Takahashi T, Kobayakawa Y, Muneoka Y, Fujisawa Y, Mohri S, Hatta M, Shimizu H, Fujisawa T, Sugiyama T, Takahara M, Yanagi K, Koizumi O (2003) Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps. Comp Biochem Physiol B Biochem Mol Biol 135:309–324

    Article  PubMed  CAS  Google Scholar 

  • Takaki M, Neya T, Nakayama S (1987) Functional role of lumbar sympathetic nerves and supraspinal mechanism in the defecation reflex of the cat. Acta Med Okayama 41:249–257

    PubMed  CAS  Google Scholar 

  • Walker RJ, Franks CJ, Pemberton D, Rogers C, Holden-Dye L (2000) Physiological and pharmacological studies on nematodes. Acta Biol Hung 51:379–394

    PubMed  CAS  Google Scholar 

  • Weinshenker D, Garriga G, Thomas JH (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. Neuroscience 15:6975–6985

    PubMed  CAS  Google Scholar 

  • Wolpert L (1971) Positional information and pattern formation. Curr Top Dev Biol 5:183–224

    Article  Google Scholar 

  • Yum S, Takahashi T, Koizumi O, Ariura Y, Kobayakawa Y, Mohri S, Fujisawa T (1998) A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Commun 248:584–590

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. H. Morishita at Hiroshima University for numerous advices and fruitful discussions about mollusks. They also wish to thank Dr. W.M. Kier at University of North Carolina and Dr. H.J. Chiel at Case Western Reserve University for providing reprints, information and encouragement. We would also like to thank Prof. R. Steele at University of California at Irvine for improving English. This research was supported by a grant from Japanese Ministry of Education to H.S (No. 60170191).

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  1. Department of Developmental Genetics, National Institute of Genetics, Mishima, Japan

    Hiroshi Shimizu

  2. Department of Anatomy, The Jikei University School of Medicine, 3-25-8, Nishi-Shinbashi, Minato-ku, Tokyo, 105-8461, Japan

    Masataka Okabe

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  1. Hiroshi Shimizu
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Correspondence to Masataka Okabe.

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Shimizu, H., Okabe, M. Evolutionary origin of autonomic regulation of physiological activities in vertebrate phyla. J Comp Physiol A 193, 1013–1019 (2007). https://doi.org/10.1007/s00359-007-0256-4

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