Summary
-
1.
Noxious cutaneous stimulation of anterior sites onAplysia californica causes withdrawal and turning followed by escape locomotion (Figs. 1, 2).
-
2.
Stimulation of anterior sites causes significantly larger turning responses than does stimulation of posterior sites (Fig. 3), so that escape locomotion is always directed away from a site of ‘attack’.
-
3.
Later phases of escape locomotion are often the same, regardless of the site of the triggering stimulus (Fig. 4).
-
4.
The defensive secretions, ink and opaline, are directed along the anterior-posterior axis at the source of noxious stimulation (Figs. 5, 6).
-
5.
Ink and opaline ejections are directed to the front or back of the animal by characteristic responses of the siphon, mantle, and parapodia (Fig. 7).
-
6.
Ink and opaline are ejected by a series of coordinated pumping movements of the mantle, gill, and parapodia that closely resemble triggered ‘respiratory pumping’ or ‘Interneuron II’ episodes (Fig. 8; Kupfermann and Kandel 1969; Byrne and Koester 1978; Hening 1982).
-
7.
The directed ejection of secretions from the mantle cavity in response to noxious stimulation suggests a number of potential defensive functions for these secretions including aggressive retaliation, startle display, diversion, and alarm signalling (Edmunds 1975).
-
8.
Taken together, our results and others' suggest an integrated scheme for the functional organization of overt defensive behavior inAplysia (Fig. 9), and begin to suggest testable hypotheses about the integration of defensive responses on the cellular level in this animal.
Similar content being viewed by others
References
Ambrose HW, Givens RP, Chen R, Ambrose KP (1979) Distastefulness as a defense mechanism inAplysia brasiliana (Mollusca: Gastropoda). Mar Behav Physiol 6:57–64
Audesirk T, Audesirk G (1985) Behavior of gastropod molluscs. In: Willows AOD (ed) Neurobiology and behavior, part 1 (The mollusca, vol 8). Academic Press, New York, pp 1–94
Beeman RD (1963) Notes on the California species ofAplysia (Gastropoda: Opisthobranchia). Veliger 5:145–147
Byrne JH (1981) Comparative aspects of neural circuits for inking behavior and gill withdrawal inAplysia californica. J Neurophysiol 45:98–106
Byrne JH (1983) Identification and initial characterization of a cluster of command and pattern-generating neurons underlying respiratory pumping inAplysia californica. J Neurophysiol 49:491–508
Byrne JH, Koester J (1978) Respiratory pumping: neuronal control of a centrally commanded behavior inAplysia. Brain Res 143:878–105
Camhi JM, Tom W (1978) The escape behavior of the cockroachPeriplaneta americana: I. Turning response to wind puffs. J Comp Physiol 128:193–201
Carew TJ, Kandel ER (1977) Inking inAplysia californica II. Central program for inking. J Neurophysiol 40:708–720
Carew TJ, Walters ET, Kandel ER (1981) Classical conditioning in a simple withdrawal reflex inAplysia californica. J Neurosci 1:1426–1437
Croll RP, (1985) Sensory control of respiratory pumping inAplysia californica. J Exp Biol 117:15–27
Eales NB (1921)Aplysia. Liverpool Marine Biol. Committee, Memoir 24. Proc Trans Liverpool Biol Soc 35:183–266
Eaton RC, Lavender WA, Wieland CM (1981) Identification of Mauthner-initiated response patterns in goldfish: Evidence from simultaneous cinematography and electrophysiology. J Comp Physiol 144:521–531
Eberly L, Kanz J, Taylor C, Pinsker H (1981) Environmental modulation of a central pattern generator in freely behavingAplysia. Behav Neural Biol 32:21–34
Eberly LB, Pinsker HM (1984) Neuroethological studies of reflex plasticity in intactAplysia. Behav Neurosci 98:609–630
Edmunds M (1975) Defence in animals. Longman, London
Erickson MT, Walters ET (1985) Directed defensive responses inAplysia californica. Soc Neurosci Abstr 11:369
Erickson MT, Walters ET (1986) Pseudoconditioning, alpha conditioning, and stimulus-response learning inAplysia. Soc Neurosci Abstr (in press)
Flury F (1915) Über das Aplysiengift. Arch Exp Pathol Pharmakol 79:250–263
Frost WN, Clark GA, Kandel ER (1985) Changes in cellular excitability in a new class of siphon motor neurons during sensitization inAplysia. Soc Neurosci Abstr 11:643
Hawkins RD, Castellucci VF, Kandel ER (1981) Interneurons involved in mediation and modulation of gill withdrawal reflex inAplysia. I. Identification and characterization. J Neurophysiol 45:304–314
Hening W (1982) Central generation and coordination of a complex behavioral sequence inAplysia californica: Locomotion and respiratory pumping. PhD dissertation, New York University
Hening W, Carew TJ, Kandel ER (1976) Interganglionic integration of different behavioral components of a centrally commanded behavior. Soc Neurosci Abstr 3:382
Hening WA, Walters ET, Carew TJ, Kandel ER (1979) Motorneuronal control of locomotion inAplysia. Brain Res 179:231–253
Jahan-Parwar B, Fredman SM (1979) Neural control of locomotion inAplysia: Role of the central ganglia. Behav Neural Biol 27:39–58
Kandel ER (1979) Behavioral biology ofAplysia. Freeman & Co., San Francisco
Kandel ER, Schwartz JH (1982) Molecular biology of learning: Modulation of transmitter release. Science 218:433–444
Kanz JE, Eberly LB, Cobbs JS, Pinsker HM (1979) Neuronal correlates of siphon withdrawal in freely behavingAplysia. J Neurophysiol 42:1538–1556
Kupfermann I, Carew TJ (1974) Behavior patterns ofAplysia californica in its natural environment. Behav Biol 12:317–337
Kupfermann I, Kandel ER (1969) Neuronal controls of a behavioral response mediated by the abdominal ganglion ofAplysia. Science 164:847–850
Kupfermann I, Pinsker H (1969) A behavioral modification of the feeding reflex inAplysia californica. Commun Behav Biol Part A 2:13–17
Kupfermann I, Weiss KR (1981) Tail-pinch and handling facilitate feeding behavior inAplysia. Behav Neural Biol 32:388–394
Kupfermann I, Carew TJ, Kandel ER (1974) Local, reflex, and central commands controlling gill and siphon movements inAplysia. J Neurophysiol 37:996–1019
MacGinitie GE, MacGinitie N (1949) Natural history of marine animals. McGraw-Hill, New York
Peretz B (1969) Central neuron initiation of periodic gill movements. Science 166:1167–1172
Perlman AJ (1979) Central and peripheral control of siphon-withdrawal inAplysia californica. J Neurophysiol 42:510–529
Pfeiffer W (1962) Alarm substances. Experientia 19:113–168
Pinsker HM, Hening WA, Carew TJ, Kandel ER (1973) Long-term sensitization of a defensive withdrawal reflex inAplysia. Science 182:1039–1042
Rayport SG, Ambron RT, Babiarz J (1983) Identified cholinergic neurons R2 and LPl1 control mucus release inAplysia. J Neurophysiol 49:864–876
Reichert H, Wine JJ (1983) Coordination of lateral giant and non-giant system in crayfish escape behavior. J Comp Physiol 153:3–15
Snedecor GW, Cochran WG (1980) Statistical Methods. Iowa State University Press, Ames, Iowa
Thompson TE (1960) Defensive adaptations in opisthobranchs. J Mar Biol Assoc UK 39:123–134
Tinbergen N (1951) The study of instinct. Clarendon Press, Oxford
Tobach E, Gold P, Ziegler A (1965) Preliminary observations of the inking behavior ofAplysia (varria) Veliger 8:16–18
Tritt SH, Byrne JH (1980) Motor controls of opaline secretion inAplysia californica. J Neurophysiol 43:581–594
Wachtel H, Impelman D (1973) A galloping escape behavior inAplysia californica. Fed Proc 32:368
Walters ET (1980) Sensitization and classical conditioning inAplysia: Behavioral and neuronal studies. Doctoral dissertation, Columbia University, New York
Walters ET (1985) Site-specific sensitization inAplysia, LTP, regenerative bursting, and a possible link in the evolution of learning. Soc Neurosci Abstr 11:795
Walters ET, Carew TJ, Kandel ER (1978) Conflict and response selection in the locomotor system ofAplysia. Soc Neurosci Abstr 4:209
Walters ET, Carew TJ, Kandel ER (1979) Classical conditioning inAplysia californica. Proc Natl Acad Sci USA 76:6675–6679
Walters ET, Carew TJ, Kandel ER (1981) Associative learning inAplysia: Evidence for conditioned fear in an invertebrate. Science 211:504–506
Walters ET, Byrne JH, Carew TJ, Kandel ER (1983) Mechanoafferent neurons innervating tail ofAplysia I. Response properties and synaptic connections. J Neurophysiol 50:1522–1542
Wine JJ, Krasne FB (1972) The organization of escape behavior in the crayfish. J Exp Biol 56:1–18
Winkler LR, Tilton BE (1962) Predation on the California sea hare,Aplysia californica Cooper, by the solitary great green sea anenome,Anthopleura xanthogrammica (Brandt), and the effect of sea hare toxin and acetylcholine on anenome muscle. Pac Sci 16:286–290
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Walters, E.T., Erickson, M.T. Directional control and the functional organization of defensive responses inAplysia . J. Comp. Physiol. 159, 339–351 (1986). https://doi.org/10.1007/BF00603980
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00603980