Skip to main content
Log in

Complex mechanoreceptors inTritonia diomedea

II. Neuronal correlates of a change in behavioral responsiveness

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    When presented with food (sea whipVirgularia sp.), a crawlingTritonia diomedea usually stops and feeds. After an escape swim, however, aTritonia crawls rapidly (the ‘escape run’) and does not stop crawling when presented with food (Fig. 1).

  2. 2.

    Complex mechanoreceptors, which are also sensitive to sea whip odor, show striking parallels with this behavior. They are normally excited by food touch, but following a swim they are much less responsive to sea whip touch (Fig. 2). Although they appear to play no role in the actual swim itself, complex receptors fire bursts of spikes during a swim in phase with ventral flexions.

  3. 3.

    If spikes are blocked in a complex receptor by injecting hyperpolarizing current during a swim (hyperpolarized swim), the change in responsiveness to sea whip touch after the swim is suppressed (Fig. 3).

  4. 4.

    Conversely, stimulating a complex receptor with short pulses of depolarizing current to produce spikes in a pattern similar to a natural swim (artificial swim) elicits a responsiveness change to sea whip touch similar to that evoked by a natural swim (Fig. 4).

  5. 5.

    The intrinsic excitability of complex receptors, as measured by the spike response to injected depolarizing current, is also changed by natural and artificial swims (Fig. 6). Suppressing spiking during swimming with hyperpolarizing current also suppresses the excitability change (Fig. 5). The excitability change after artificial swims persists when interneuronal firing is suppressed with high Ca++ (Fig. 7) and high Mg++, high Ca++ solutions.

  6. 6.

    It is concluded that the receptor responsiveness change following a swim is produced by the spiking or depolarization of the individual receptor which occurs during a swim. This receptor change may in turn contribute to the behavioral change seen in the intact animal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alkon, D.L.: Associative training ofHermissenda. J. Gen. Physiol.64, 70–84 (1974)

    Google Scholar 

  • Alkon, D.L.: Neural correlates of associative training inHermissenda. J. Gen. Physiol.65, 46–56 (1975)

    Google Scholar 

  • Alkon, D.L.: Neural modification by paired sensory stimuli. J. Gen. Physiol.68, 341–358 (1976)

    Google Scholar 

  • Alkon, D.L.: Voltage-dependent calcium and potassium ion conductances: A contingency mechanism for an associative learning model. Science205, 810–816 (1979)

    Google Scholar 

  • Audesirk. G.: Central neuronal control of cilia inTritonia diomedea. Nature272, 541–543 (1978a)

    Google Scholar 

  • Audesirk, G.: Properties of central motor neurons exciting locomotory cilia inTritonia diomedea. J. Comp. Physiol.128, 259–267 (1978b)

    Google Scholar 

  • Audesirk, G., Audesirk, T.: Complex receptors inTritonia: Neural correlates of a change in behavioral responsiveness. Soc. Neurosci. Abs.5, 240 (1979a)

    Google Scholar 

  • Audesirk, G., Audesirk, T.: Complex mechanoreceptors inTritonia diomedea. I. Responses to mechanical and chemical stimuli. J. Comp. Physiol.141, 101–109 (1980)

    Google Scholar 

  • Audesirk, T., Audesirk, G.: Oral mechanoreceptors inTritonia diomedea. II. Role in feeding. J. Comp. Physiol.130, 79–86 (1979b)

    Google Scholar 

  • Baylor, D.A., Nicholls, J.G.: After-effects of nerve impulses on signalling in the central nervous system of the leech. J. Physiol.203, 571–589 (1969)

    Google Scholar 

  • Brodwick, M.S., Junge, D.: Post-stimulus hyperpolarization and slow potassium conductance increase inAplysia giant neurone. J. Physiol.223, 549–570 (1972)

    Google Scholar 

  • Byrne, J.H., Koester, J.: Respiratory pumping: neuronal control of a centrally commanded behavior inAplysia. Brain Res.143, 87–105 (1978)

    Google Scholar 

  • Castellucci, V.F., Pinsker, H., Kupfermann, I., Kandel, E.R.: Neuronal mechanism of habituation and dishabituation of the gill withdrawal reflex ofAplysia. Science167, 1745–1748 (1970)

    Google Scholar 

  • Castellucci, V.F., Carew, T.J., Kandel, E.R.: Cellular analysis of long-term habituation of the gill-withdrawal reflex ofAplysia californica. Science202, 1306–1308 (1978)

    Google Scholar 

  • Chang, J.J., Gelperin, A.: Learned modification of a molluscan feeding response produced in the isolated central nervous system. Soc. Neurosci. Abs.4, 189 (1978)

    Google Scholar 

  • Crow, T.J., Alkon, D.L.: Retention of an associative behavioral change inHermissenda. Science201, 1239–1241 (1978)

    Google Scholar 

  • Davis, W.J., Gillette, R.: Neural correlate of behavioral plasticity in command neurons ofPleurobranchaea. Science199, 801–804 (1978)

    Google Scholar 

  • Davis, W.J., Mpitsos, G.J., Pinneo, J.M.: The behavioral hierarchy of the molluscPleurobranchaea. I. The dominant position of the feeding behavior. J. Comp. Physiol.90, 207–224 (1974a)

    Google Scholar 

  • Davis, W.J., Siegler, M.V.L., Pinneo, J.M., Davis, K.B.: Neuronal substrates of behavioral hierarchies and associative learning inPleurobranchaea. Am. Zool.13, 1037–1049 (1974b)

    Google Scholar 

  • Gage, P.W., Hubbard, J.I.: The origin of the post-tetanic hyperpolarization of mammalian motor nerve termina. J. Physiol.184, 335–352 (1966)

    Google Scholar 

  • Gelperin, A.: Rapid food-aversion learning in a terrestrial mollusk. Science189, 567–570 (1975)

    Google Scholar 

  • Gustafsson, B., Lindström, S., Takata, M.: Afterhyperpolarization mechanism in the dorsal spinocerebellar tract cells of the cat. J. Physiol.275, 283–301 (1978)

    Google Scholar 

  • Junge, D.: Increased K-conductance as proximate cause of poststimulus hyperpolarization inTritonia neurones. Comp. Biochem. Physiol.42A, 975–981 (1972)

    Google Scholar 

  • Kovac, M.P., Davis, W.J.: Reciprocal inhibition between distinct behavioral acts inPleurobranchaea. Soc. Neurosci. Abs.5, 250 (1979)

    Google Scholar 

  • Kuno, M., Miyahara, J.T., Weakly, J.N.: Post-tetanic hyperpolarization produced by an electrogenic pump in dorsal spinocerebellar tract neurones of the cat. J. Physiol.210, 839–855 (1970)

    Google Scholar 

  • Kupfermann, I., Castellucci, V.F., Pinsker, H., Kandel, E.R.: Neuronal correlates of habituation and dishabituation of the gillwithdrawal reflex ofAplysia. Science167, 1743–1745 (1970)

    Google Scholar 

  • Lukowiak, K., Jacklet, J.: Habituation and dishabituation: Interactions between peripheral and central nervous systems inAplysia. Science178, 1306–1308 (1972)

    Google Scholar 

  • Lukowiak, K., Jacklet, J.: Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon ofAplysia. J. Neurobiol.6, 182–200 (1975)

    Google Scholar 

  • Lukowiak, K., Peretz, B.: The interaction between the central and peripheral nervous systems in the mediation of gill withdrawal reflex behavior inAplysia. J. Comp. Physiol.117, 219–244 (1977)

    Google Scholar 

  • Mpitsos, G.J., Collins, S.: Learning: Rapid aversive conditioning in the gastropodPleurobranchaea. Science188, 954–957 (1975)

    Google Scholar 

  • Mpitsos, G.J., Davis, W.J.: Classical and avoidance conditioning in the molluskPleurobranchaea. Science180, 317–320 (1973)

    Google Scholar 

  • Mpitsos, G.J., Collins, S., McClellan, A.D.: Learning: A model system for physiological studies. Science199, 497–506 (1978)

    Google Scholar 

  • Peretz, B.: Habituation and dishabituation in the absence of the central nervous system. Science169, 379–381 (1970)

    Google Scholar 

  • Peretz, B., Jacklet, J., Lukowiak, K.: Habituation of reflexes inAplysia: Contribution of the peripheral and central nervous system. Science191, 396–199 (1976)

    Google Scholar 

  • Pinsker, H., Kupfermann, I., Castellucci, V.F., Kandel, E.R.: Habituation and dishabituation of the gill-withdrawal reflex inAplysia. Science167, 1740–1742 (1970)

    Google Scholar 

  • Ram, J.L., Davis, W.J.: Mechanisms underlying “singleness of action” in the feeding behavior ofPleurobranchaea californica (MacFarland, 1966). Veliger20, 55–56 (1978)

    Google Scholar 

  • Sokolove, P.G., Cooke, I.M.: Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J. Gen. Physiol.57, 125–163 (1971)

    Google Scholar 

  • Stephens, C.L.: Progressive decrements in the activity ofAplysia neurones following repeated intracellular stimulation: implications for habituation. J. Exp. Biol.58, 411–421 (1973a)

    Google Scholar 

  • Stephens, C.L.: Relative contribution of synaptic and non-synaptic influences to response decrements in a post-synaptic neurone. J. Exp. Biol.59, 315–321 (1973b)

    Google Scholar 

  • Wachtel, H., Kandel, E.R.: Conversion of synaptic excitation to inhibition at a dual chemical synapse. J. Neurophysiol.34, 56–68 (1971)

    Google Scholar 

  • Willows, A.O.D.: Physiology of feeding inTritonia. I. Behavior and mechanics. Mar. Behav. Physiol.5, 115–135 (1978)

    Google Scholar 

  • Willows, A.O.D., Hoyle, G.: Neuronal network triggering a fixed action pattern. Science166, 1549–1551 (1969)

    Google Scholar 

  • Willows, A.O.D., Dorsett, D.A., Hoyle, G.: The neuronal basis of behavior inTritonia. I. Functional organization of the central nervous system. J. Neurobiol.4, 207–237 (1973)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by NSF Research Grant BMS 75613579 to A.O.D. Willows, and by NIH National Research Service Awards 1-F32-NS05388-01A1 to Teresa Audesirk and 5-F32-NS05151 to Gerald Audesirk. We would like to thank Dennis Willows and Patricia Dickinson for helpful discussions in the course of this research, and William Stark for critical reading of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Audesirk, G., Audesirk, T. Complex mechanoreceptors inTritonia diomedea . J. Comp. Physiol. 141, 111–122 (1980). https://doi.org/10.1007/BF00611884

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00611884

Keywords

Navigation