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Humoral factors released during trauma ofAplysia body wall

I. Body wall contraction, cardiac modulation, and central reflex suppression

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Summary

  1. 1.

    Mechanical or electrical stimulation of isolated sections of body wall produced contractions that were graded with the intensity of the stimulus. Injury of body wall with shallow incisions produced extremely persistent contractions.

  2. 2.

    Long-lasting contraction of isolated body wall was also produced by brief application of “stimulated body wall wash” (SBW), sea water which was first washed through another section of body wall subjected to intense mechanical or electrical stimulation. Contractions were produced by SBW diluted to concentrations as low as 1% of the initial concentration. Contractions produced by prolonged application of SBW showed little fatigue, tachyphylaxis, or desensitization.

  3. 3.

    SBW caused contraction of isolated sections of body wall from all regions of the body, including tail, parapodia, siphon, purple gland, rhinophores, and anterior tentacles. SBW also caused contraction of isolated lateral columellar muscle and of the gill.

  4. 4.

    30 mM CoCl2 blocked the release of contractile factors into electrically stimulated body wall and reduced but did not abolish contractile responses of unstimulated body wall to perfused SBW. SBW contractions were unchanged by disconnection of the perfused tissue to the CNS.

  5. 5.

    Hemolymph collected from the neck of an intact donor following strong electrical stimulation of the tail or excision of a parapodium (‘stimulated hemolymph’, SHL) caused long-lasting contractions which were larger than those produced by control hemolymph (CHL) collected prior to stimulation of the donor.

  6. 6.

    Similarities between body wall contractions produced by SHL and by SBW, including their occurrence in 30 mM CoCl2, suggest that some of the contractile activity in SHL may be directly released from traumatized body wall.

  7. 7.

    SHL caused significantly greater cardioacceleration of the isolated heart than did CHL. Similarities between the cardioacceleration produced by SHL and by SBW suggest that a source of cardiac activity in SHL may be traumatized body wall.

  8. 8.

    SBW suppressed the gill-withdrawal reflex when applied selectively to the sheathed or desheathed abdominal ganglion. SBW-induced suppression was associated with significant reduction of evoked spike activity in identified gill motor neurons. SHL collected 1–2 h after noxious stimulation caused weak but significant suppression of the gill-withdrawal reflex when applied to the fully sheathed abdominal ganglion.

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Abbreviations

ASW :

artificial seawater

CBW :

control body wall wash

SBW :

stimulated body wall wash

CHL :

control hemolymph

SHL :

stimulated hemolymph

References

  • Abrams TW, Castellucci VF, Kandel ER, Lloyd PE (1984) Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex inAplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel. Proc Natl Acad Sci USA 81:7956–7960

    Google Scholar 

  • Arch S (1976) Neuroendocrine regulation of egg laying inAplysia californica. Am Zool 16:167–175

    Google Scholar 

  • Bablanian GM, Treistman SN (1985) The effect of hyperpolarization of cell R15 on the hemolymph composition of intactAplysia. J Comp Physiol B 155:297–303

    Google Scholar 

  • Bailey CH, Castellucci VF, Koester J, Kandel ER (1979) Cellular studies of peripheral neurons in siphon skin ofAplysia californica. J Neurophysiol 42:530–557

    Google Scholar 

  • Bayne CJ (1983) Molluscan immunobiology. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 5: Physiology, part 2. Academic Press, New York, pp 407–486

    Google Scholar 

  • Besson J-M, Chaouch A (1987) Peripheral and spinal mechanisms of nociception. Physiol Rev 67:67–186

    Google Scholar 

  • Billy AJ, Walters ET (1989) Long-term expansion and sensitization of mechanosensory receptive fields inAplysia support an activity-dependent model of whole-cell plasticity. J Neurosci 9:1254–1262

    Google Scholar 

  • Bodnar RJ (1986) Neuropharmacological and neuroendocrine substrates of stress-induced analgesia. Ann NY Acad Sci 467:345–360

    Google Scholar 

  • Brace RC (1977) The functional anatomy of the mantle complex and columellar muscle of tectibranch molluses (Gastropoda: Opisthobranchia) and its bearing on the evolution of opisthobranch organization. Phil Trans R Soc London (B) 277:1–56

    Google Scholar 

  • Byrne JH, Shapiro E, Dieringer N, Koester J (1979) Biophysical mechanisms contributing to inking behavior inAplysia. J Neurophysiol 42:1233–1250

    Google Scholar 

  • Carew TJ, Pinsker H, Rubinson K, Kandel ER (1974) Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle inAplysia. J Neurophysiol 37:1020–1040

    Google Scholar 

  • Chiu AY, Hunkapiller MW, Heller E, Stuart DK, Hood LE, Strumwasser F (1979) Purification and primary structure of the neuropeptide egg-laying hormone ofAplysia californica. Proc Natl Acad Sci USA 76:6656–6660

    Google Scholar 

  • Clowes GHA (1988) Stresses, meciators, and responses of survival. In: Clowes GHA (ed) Trauma, sepsis, and shock. Marcel Dekker, New York, pp 1–53

    Google Scholar 

  • Cooper BF, Krontiris-Litowitz JK, Walters ET (1986) Properties of humoral factor(s) released fromAplysia body wall by sensitizing stimulation. Soc Neurosci Abstr 12:861

    Google Scholar 

  • Cooper BF, Krontiris-Litowitz JK, Walters ET (1989) Humoral factors released during trauma ofAplysia body wall. II. Effects of possible mediators. J Comp Physiol B 159:225–235

    Google Scholar 

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

    Google Scholar 

  • Dillon PF, Aksoy MO, Driska SP, Murphey RA (1981) Myosin phosphorylation and the crossbridge cycle in arterial smooth muscle. Science 211:495–497

    Google Scholar 

  • Hoyle G (1983) Muscles and their neural control. Wiley, New York

    Google Scholar 

  • Jones HD (1983) The circulatory systems of gastropods and bivalves. In: Saleuddin ASM, Wilbur KM (eds). The Mollusca, vol 5: Physiology, part 2. Academic Press, New York, pp 189–238

    Google Scholar 

  • Joose J, Geraerts WPM (1983) Endocrinology. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 4: Physiology, part 1. Academic Press, New York, pp 317–406

    Google Scholar 

  • Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433–444

    Google Scholar 

  • Kavaliers MP (1987) Evidence for opioid and non-opioid forms of stress-induced analgesia in the snail,Cepaea nemoralis. Brain Res 410:111–115

    Google Scholar 

  • Klein M, Kandel ER (1978) Presynaptic modulation of voltage-dependent Ca2+ current: mechanism for behavioral sensitization inAplysia californica. Proc Natl Acad Sci USA 75:3512–3516

    Google Scholar 

  • Kravitz EA, Beltz B, Glusman S, Goy M, Harris-Warrick R, Johnston M, Livingstone M, Schwarz T, Siwicki KK (1985) The well modulated lobster. The roles of serotonin, octopamine, and proctolin in the lobster nervous system. In: Selverstor (ed) Model neural networks and behavior. Plenum Press, New York, pp 339–360

    Google Scholar 

  • Krieger DT (1983) Brain peptides: what, where, and why? Science 222:975–986

    Google Scholar 

  • Krontiris-Litowitz JK, Cooper BF, Walters ET (1986) Hemolymph from sensitizedAplysia modulates body wall tension and heart rate. Soc Neurosci Abstr 12:861

    Google Scholar 

  • Krontiris-Litowitz JK, Erickson MT, Walters ET (1987) Central suppression of defensive reflexes by noxious stimulation and by factors released from body wall. Soc Neurosci Abstr 13:815

    Google Scholar 

  • Kupfermann I (1967) Stimulation of egg laying: possible endocrine function of bag cells of abdominal ganglion ofAplysia californica. Nature 216:814–815

    Google Scholar 

  • Kupfermann I, Carew TJ, Kandel ER (1974) Local, reflex, and central commands controlling gill and siphon movements inAplysia. J Neurophysiol 37:996–1019

    Google Scholar 

  • Lukowiak K (1987) A blood-borne factor from food-satiatedAplysia suppresses the gill withdrawal reflex in in vitro preparations from unsatiated animals. Neurosci Lett 77:205–208

    Google Scholar 

  • Mackey SL, Glanzman DL, Small SA, Dyke AM, Kandel ER, Hawkins RD (1987) Tail shock produces inhibition as well as sensitization of the siphon-withdrawal reflex ofAplysia: possible behavioral role for presynaptic inhibition mediated by the peptide Phe-Met-Arg-Phe-NH2. Proc Natl Acad Sci USA 84:8730–8734

    Google Scholar 

  • Marcus EA, Nolen TG, Rankin CH, Carew TJ (1988) Behavioral dissociation of dishabituation, sensitization and inhibition inAplysia. Science 241:210–213

    Google Scholar 

  • Martin AW, Harrison FM, Huston MJ, Stewart DM (1958) The blood volumes of some representative molluscs. J Exp Biol 35:260–279

    Google Scholar 

  • Mason JW (1968) Organization of the multiple endocrine responses to avoidance in the monkey. Psychosomatic Med 30:774–790

    Google Scholar 

  • Mattson MP, Spaziani E (1985) Stress reduces hemolymph ecdysteroid levels in the crab: mediation by the eyestalks. J Exp Zool 234:319–323

    Google Scholar 

  • Nolen TG, Carew TJ (1987) Analysis of non-decremented EPSPs prior to the emergence of sensitization reveals an inhibitory process inAplysia. Soc Neurosci Abstr 13:816

    Google Scholar 

  • Pierce SK (1971) A source of solute for volume regulation in marine mussels. Comp Biochem Physiol 38A:619–635

    Google Scholar 

  • Ram JL, Shukla UA, Parti R, Goines RL (1984) Extracellular Ca2+ dependence of contracture and modulation by serotonin in buccal muscle E1 ofAplysia. J Neurobiol 3:197–206

    Google Scholar 

  • Reilly WM, Peretz B (1987) Excitation-contraction coupling in non-spiking smooth muscle in the gill ofAplysia. J Comp Physiol B 157:659–666

    Google Scholar 

  • Roth J, LeRoith D, Shiioach J, Rosenzweig JL, Lesniak MA, Havrankova J (1982) The evolutionary origins of hormones, neurotransmitters, and other extracellular chemical messengers. New Eng J Med 306:523–527

    Google Scholar 

  • Sminia T, Pietersma K, Scheerboom JEM (1973) Histological and ultrastructural observations on woud healing in the freshwater pulmonatelymnaea stagnalis. Z Zellforsch 141:561–573

    Google Scholar 

  • Smith PJS (1987) Cardiac output in the Mollusca: scope and regulation. Experientia 43:956–965

    Google Scholar 

  • Sugi H, Yamaguchi T (1976) Activation of the contractile mechanism in the anterior byssal retractor muscle ofMytilus edulis. J Physiol 257:531–547

    Google Scholar 

  • Twarog BM (1976) Aspects of smooth muscle function in molluscan catch muscle. Physiol Rev 56:829–838

    Google Scholar 

  • Walters ET (1987a) Site-specific sensitization of defensive reflexes inAplysia: A simple model of long-term hyperalgesia. J Neurosci 7:400–407

    Google Scholar 

  • Walters ET (1987b) Multiple sensory neuronal correlates of site-specific sensitization inAplysia. J Neurosci 7:408–417

    Google Scholar 

  • Walters ET, Erickson MT (1986) Directional control and the functional organization of defensive responses inAplysia. J Comp Physiol A 159:339–351

    Google Scholar 

  • Walters ET, Byrne JH, Carew TJ, Kandel ER (1983a) Mechanoafferent neurons innervating tail ofAplysia. I. Response properties and synaptic connections. J Neurophysiol 50:1522–1542

    Google Scholar 

  • Walters ET, Byrne JH, Carew TJ, Kandel ER (1983b) Mechanoafferent neurons innervating tail ofAplysia. II. Modulation by sensitizing stimulation. J Neurophysiol 50:1543–1559

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology and Cell Biology, University of Texas Medical School at Houston, 77225, Houston, Texas, USA

    Johanna K. Krontiris-Litowitz, Bruce F. Cooper & Edgar T. Walters

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  1. Johanna K. Krontiris-Litowitz
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  2. Bruce F. Cooper
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  3. Edgar T. Walters
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Krontiris-Litowitz, J.K., Cooper, B.F. & Walters, E.T. Humoral factors released during trauma ofAplysia body wall. J Comp Physiol B 159, 211–223 (1989). https://doi.org/10.1007/BF00691742

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