Advertisement

Journal of Comparative Physiology A

, Volume 193, Issue 10, pp 1013–1019 | Cite as

Evolutionary origin of autonomic regulation of physiological activities in vertebrate phyla

  • Hiroshi Shimizu
  • Masataka OkabeEmail author
Review

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.

Keywords

Autonomic nervous system Heart rate Fight or flight response Sympathetic nervous system Parasympathetic nervous system 

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

Notes

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).

References

  1. Albertson DG, Thomson JU (1976) The pharynx of Caenohabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:299–325PubMedCrossRefGoogle Scholar
  2. Avery L (1993) Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. J Exp Biol 175:283–297PubMedGoogle Scholar
  3. Avery L, Horvitz HR (1989) Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of Caenorhabditis elegans. Neuron 3:473–485PubMedCrossRefGoogle Scholar
  4. Bodmer R (1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–729PubMedGoogle Scholar
  5. 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 YorkGoogle Scholar
  6. Cannon WB (1932) The wisdom of the body. Kegan Paul, LondonGoogle Scholar
  7. Chen JN, Fishman MC (2000) Genetics of heart development. Trends Genet 16:383–388PubMedCrossRefGoogle Scholar
  8. Crick F (1970) Diffusion in embryogenesis. Nature 231:420–422CrossRefGoogle Scholar
  9. Dieringer N, Koester J, Weiss KR (1978) Adaptive changes in heart rate of Aplysia californica. J Comp Physiol 123:11–21CrossRefGoogle Scholar
  10. 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 200:735–752PubMedGoogle Scholar
  11. Ellis CH (1944) The mechanism of extension in the legs of spiders. Biol Bull 86:41–50CrossRefGoogle Scholar
  12. Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193PubMedGoogle Scholar
  13. Ganong WF (1999) Review of medical physiology. 19th edn. McGraw-Hill Medical Publishing, New YorkGoogle Scholar
  14. Gershon MD, Erde SM (1981) The nervous system of the gut. Gastroenterology 80:1571–1594PubMedGoogle Scholar
  15. Goldstein R, Kistler HB Jr, Steinbusch HWM, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. Neurosci 11:535–547CrossRefGoogle Scholar
  16. 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 180:473–488PubMedCrossRefGoogle Scholar
  17. 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 126:517–524PubMedGoogle Scholar
  18. Hukuhara T, Yamagami M, Nakayama S (1958) On the intestinal intrinsic reflexes. Jpn J Physiol 8:9–20PubMedGoogle Scholar
  19. 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 11:281–288PubMedGoogle Scholar
  20. 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 11:635–640PubMedGoogle Scholar
  21. 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 211–252Google Scholar
  22. Kier WM, Smith KK (1985) Tongues, tentacles and trunks: The biomechanics of movement in muscular-hydrostats. Zool J Linn Soc 83:307–324Google Scholar
  23. Koch UT, Koester J, Weiss KR (1984) Neuronal mediation of cardiovascular effects of food arousal in Aplysia. J Neurophysiol 51:126–135PubMedGoogle Scholar
  24. Koester J, Koch UT (1984) Neural control of the circulatory system of Aplysia. Experientia 43:972–980CrossRefGoogle Scholar
  25. Kupfermann I (1991) Functional studies of cotransmission. Physiol Rev 71:683–732PubMedGoogle Scholar
  26. Lenhoff HM (1961) Digestion of ingested protein by Hydra as studied by radioautography and fractionation by differential solubilities. Exp Cell Res 23:335–353PubMedCrossRefGoogle Scholar
  27. 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 119:419–431PubMedGoogle Scholar
  28. Marcum BA, Campbell RD (1978) Development of Hydra lacking nerve and interstitial cells. J Cell Sci. 29:17–33PubMedGoogle Scholar
  29. Matthews GG (1997) Neurobiology: molecules, cells, and systems. Blackwell, New York, pp 23–24Google Scholar
  30. Meinhardt H (1997) Models of biological pattern formation. Academic, New YorkGoogle Scholar
  31. Meinhardt H (2002) The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. Bioessays 24:185–191PubMedCrossRefGoogle Scholar
  32. 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 207:189–203PubMedCrossRefGoogle Scholar
  33. Moosler A, Rinehart KL, Grimmelikhuijzen CJP (1996) Isolation of four novel neuropeptides, the Hydra RFamides I-IV, from Hydra magnipapillata. Biochem Biophys Res Commun 229:596–602PubMedCrossRefGoogle Scholar
  34. Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C, Smeets WJAJ (1998) The central nervous system of vertebrates: an introduction to structure and function. Springer HeidelbergGoogle Scholar
  35. 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 124:3965–3973PubMedGoogle Scholar
  36. Ono JK, McCaman RE (1984) Immunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia. Neuroscience 11:549–560PubMedCrossRefGoogle Scholar
  37. Parry DA, Brown RHJ (1959) The hydraulic mechanism of the spider leg. J Exp Biol 36:423–433Google Scholar
  38. Pennisi E (2003) Drafting a tree. Science 300:1694PubMedCrossRefGoogle Scholar
  39. Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671PubMedCrossRefGoogle Scholar
  40. Ram JL, Shukla UA, Ajimal GS (1981) Serotonin has both excitatory and inhibitory modulatory effects on feeding muscle in Aplysia. J Neurobiol 12:613–621PubMedCrossRefGoogle Scholar
  41. Riddle DL, Blumenthal T, Meyer BJ, Priess JR (1997) C. elegans II: monograph 33 (Cold Spring Harbor Monograph Series) Cold Spring Harbor Laboratory PressGoogle Scholar
  42. Robertson D, Low PA, Polinsky RJ (1996) Primer on the autonomic nervous system. Academic, San DiegoGoogle Scholar
  43. Ruppert EE, Barnes RD (1996) Invertebrate zoology. Saunders College, Fort Worth Google Scholar
  44. Sakaguchi M, Mizusina A, Kobayakawa Y (1996) Structure, development, and maintenance of the nerve net of the body column in Hydra. J Comp Neurol 373:41–54PubMedCrossRefGoogle Scholar
  45. Sarnat HB, Netsky MG (2002) When does a ganglion become a brain? Evolutionary origin of the central nervous system. Semin Pediatr Neurol 9:240–253PubMedCrossRefGoogle Scholar
  46. 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 26:619–631PubMedCrossRefGoogle Scholar
  47. Shimizu H, Fujisawa T (2003) Peduncle of Hydra and the heart of higher organisms share a common ancestral origin. genesis 36:182–186PubMedCrossRefGoogle Scholar
  48. 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 190:623–630CrossRefGoogle Scholar
  49. Sugden AM, Jasny BR, Culotta E, Pennisi E (2003) Charting the evolutionary history of life. Science 300:1691CrossRefGoogle Scholar
  50. 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 19:187–200CrossRefGoogle Scholar
  51. 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 135:309–324PubMedCrossRefGoogle Scholar
  52. 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 41:249–257PubMedGoogle Scholar
  53. Walker RJ, Franks CJ, Pemberton D, Rogers C, Holden-Dye L (2000) Physiological and pharmacological studies on nematodes. Acta Biol Hung 51:379–394PubMedGoogle Scholar
  54. Weinshenker D, Garriga G, Thomas JH (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. Neuroscience 15:6975–6985PubMedGoogle Scholar
  55. Wolpert L (1971) Positional information and pattern formation. Curr Top Dev Biol 5:183–224CrossRefGoogle Scholar
  56. 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 248:584–590PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Developmental GeneticsNational Institute of GeneticsMishimaJapan
  2. 2.Department of AnatomyThe Jikei University School of MedicineTokyoJapan

Personalised recommendations