Journal of Comparative Physiology A

, Volume 172, Issue 2, pp 153–169

Cerebral neurons underlying prey capture movements in the pteropod mollusc, Clione limacina

I. Physiology, morphology
  • T. P. Norekian
  • R. A. Satterlie


The pteropod mollusc Clione limacina feeds on shelled pteropods capturing them with 3 pairs of oral appendages, called buccal cones. A group of electricallycoupled putative motoneurons (A neurons) has been identified in the cerebral ganglia, whose activation induces opening of the oral skin folds and extrusion of the buccal cones. These cells are normally silent and have one or two axons in the ipsilateral head nerves. Electrical coupling between A neurons is relatively weak and normally does not produce 1∶1 spike synchronization. Coupling coefficients ranged from 0.05 to 0.25.

A second type of putative motoneurons (B neurons) controls retraction and withdrawal of buccal cones. B neurons show spontaneous spike activity which maintains the buccal cones in a continuous retracted state. All B neurons have one axon running into the head nerves. Ipsilateral B motoneurons are electrically coupled to each other. A neurons strongly inhibit B neurons, however, seven identified A motoneurons which were specifically tested do not form monosynaptic contacts with B motoneurons.

Appropriate stimuli from the prey activate A motoneurons, which in turn inhibit B motoneurons and evoke extrusion of the buccal cones. One mechanism promoting the speed of this extremely rapid reaction is brief co-activation of antagonistic A and B neuron groups, which provides a notable increase in fluid pressure inside the head.

Mechanical stimulation of buccal cones provides excitatory inputs to A motoneurons. Similar stimulation from captured prey would serve to prolong buccal cone protraction during the manipulatory phase of feeding.

Key words

Mollusc Feeding Cerebral motoneurons Electrical coupling 


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  1. Anderson PAV, Mackie GO (1977) Electrically coupled, photosensitive neurons control swimming in a jellyfish. Science 197:186–188Google Scholar
  2. Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985) Control of locomotion in marine mollusc Clione limacina II. Rhythmic neurons of pedal ganglia. Exp Brain Res 58:263–272Google Scholar
  3. Benjamin PR (1983) Gastropod feeding: behavioral and neural analysis of a complex multicomponent system. In: Roberts A, Roberts B (eds) Neural origin of rhythmic movements. Cambridge University Press, Cambridge, pp 159–193Google Scholar
  4. Benjamin PR, Rose RM (1979) Central generation of bursting in the feeding system of the snail, Lymnaea stagnalis. J Exp Biol 80:93–118Google Scholar
  5. Bennett MVL (1972) A comparison of electrically and chemically mediated transmission. In: Pappas GD, Purpura DP (eds) Structure and function of synapses. Raven Press, New York, pp 221–256Google Scholar
  6. Bennett MVL (1974) Flexibility and rigidity in electrotonically coupled systems. In: Bennett MVL (ed) Synaptic transmission and neuronal interaction. Raven Press, New York, pp 153–178Google Scholar
  7. Berry MS (1972a) A system of electrically coupled small cells in the buccal ganglia of the pond snail Planorbis corneus. J Exp Biol 56:621–637Google Scholar
  8. Berry MS (1972b) Electrotonic coupling between identified large cells in the buccal ganglia of Planorbis corneus. J Exp Biol 57:173–185Google Scholar
  9. Carew TJ, Kandel ER (1976) Two functional effects of decreased conductance EPSP's: synaptic augmentation and increased electrotonic coupling. Science 192:150–153Google Scholar
  10. Davis WJ, Mpitsos GJ (1971) Behavioral choice and habituation in the marine mollusk Pleurobranchaea californica MacFarland (Gastropoda, Opisthobranchia). Z Vergl Physiol 75:207–232Google Scholar
  11. Davis WJ, Mpitsos GJ, Pinneo JM (1974) The behavioral hierarchy of the mollusk Pleurobranchaea. I. The dominant position of the feeding behavior. J Comp Physiol 90:207–224Google Scholar
  12. Dyakonova TL, Moroz LL, Winlow W (1991) Facilitation of electrical coupling between identified central neurons by met-enkephalin in Helix and Lymnaea. J Physiol (Lond) 438:283Google Scholar
  13. Ferguson GP, Benjamin P (1991) The whole-body withdrawal response of Lymnaea stagnalis. I. Identification of central motoneurones and muscles. J Exp Biol 158:63–95Google Scholar
  14. Gardner D (1971) Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia. Science 173:550–553Google Scholar
  15. Getting PA (1974) Modification of neuron properties by electrotonic synapses. I. Input resistance, time constant, and integration. J Neurophysiol 37:846–857Google Scholar
  16. Heitler WJ, Burrows M (1977) The locust jump. I. The motor programme. J Exp Biol 66:203–219Google Scholar
  17. Hermans CO, Satterlie RA (1992) Fast-strike feeding behavior in a pteropod mollusc, Clione limacina Phipps. Biol Bull 182:1–7Google Scholar
  18. Kaneko CRS, Merickel M, Kater SB (1978) Centrally programmed feeding in Helisoma: Identification and characteristics of an electrically coupled premotor neuron network. Brain Res 146:1–21Google Scholar
  19. Kater SB (1974) Feeding in Helisoma trivolvis: The morphological and physiological bases of a fixed action pattern. Am Zoologist 14:1017–1036Google Scholar
  20. Koester J (1989) Chemically and electrically coupled interneurons mediate respiratory pumping in Aplysia. J Neurophysiol 62:1113–1126Google Scholar
  21. Kohn AJ (1983) Feeding biology of Gastropods. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, Vol. 5, Physiology, Part 2. Academic Press, New York, pp 1–63Google Scholar
  22. Kupfermann I (1974) Feeding behavior in Aplysia: A simple system for the study of motivation. Behav Biol 10:1–26Google Scholar
  23. Lalli CM, Gilmer RW (1989) Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford, Stanford Univ PressGoogle Scholar
  24. Levitan H, Tauc L, Segundo JP (1970) Electrical transmission among neurons in the buccal ganglion of a mollusc, Navanax inermis. J Gen Physiol 55:484–496Google Scholar
  25. Litvinova NM, Orlovsky GN (1985) Feeding behaviour of pteropod mollusc Clione limacina. Bull Soc Nat Moscow, Sect Biol 90:73–77 (in Russian)Google Scholar
  26. Murray MJ (1977) Predatory behavior in Navanax inermis. Veliger 20:55Google Scholar
  27. Norekian TP, Satterlie RA (1991a) Acquisition phase of feeding behavior in the pteropod mollusc, Clione limacina. Soc Neurosci Abstr 17:1593Google Scholar
  28. Norekian TP, Satterlie RA (1991b) Neuronal analysis of hunting behavior of the pteropod mollusc, Clione limacina. J High Nerv Activ 41:982–997 (in Russian)Google Scholar
  29. Nusbaum MP, Friesen WO, Kristan WB Jr, Pearce RA (1987) Neuronal mechanisms generating the leech swimming rhythm: swim-initiator neurons excite the network of swim oscillator neurons. J Comp Physiol A 161:355–366Google Scholar
  30. Rao G, Barnes CA, McNaughton BL (1986) Intracellular fluorescent staining with carboxyfluorescein: a rapid and reliable method for quantifying dye-coupling in mammalian central nervous system. J Neurosci Meth 16:251–263Google Scholar
  31. Sakharov DA, Kabotyansky EA (1986) Integration of behavior of a pteropod mollusc by dopamine and serotonin. Zh Obshch Biol 47:234–245 (in Russian)Google Scholar
  32. Satterlie RA (1989) Reciprocal inhibition and rhythmicity: swimming in a pteropod mollusk. In: Jacklet JW (ed) Neuronal and Cellular Oscillators. Marcel Dekker Inc., New York Basel, pp 151–171Google Scholar
  33. Satterlie RA, Spencer AN (1983) Neuronal control of locomotion in hydrozoan medusae. J Comp Physiol 150:195–206Google Scholar
  34. Spencer AN (1981) The parameters and properties of a group of electrically coupled neurones in the central nervous system of a hydrozoan jellyfish. J Exp Biol 93:33–50Google Scholar
  35. Spira ME, Bennett MVL (1972) Synaptic control of electrotonic coupling between neurons. Brain Res 37:294–300Google Scholar
  36. Spira ME, Spray DC, Bennett MVL (1980) Synaptic organization of expansion motorneurons of Navanax inermis. Brain Res 195:241–269Google Scholar
  37. Susswein AJ, Achituv Y, Cappell MS, Spray DC, Bennett MVL (1984) Pharyngeal movements during feeding sequences in Navanax inermis: A cinematographic analysis. J Comp Physiol A 155:209–218Google Scholar
  38. Syed NI, Winlow W (1991) Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J Exp Biol 158:37–62Google Scholar
  39. Wagner N (1885) Die Wirbellosen des Weissen Meeres: Zoologische Forschungen an der Küste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre. Verlag Von Wilhelm Engelmann, LeipzigGoogle Scholar
  40. Willows AOD, Hoyle G (1969) Neuronal network triggering a fixed action pattern. Science 166:1549–1551Google Scholar
  41. Zakharov IS, Ierusalimsky VN (1992) The neuroanatomical basis of feeding behavior in the pteropod mollusc, Clione limacina (Phipps). J Comp Physiol A 170:525–532Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • T. P. Norekian
    • 1
    • 2
  • R. A. Satterlie
    • 1
    • 2
  1. 1.Friday Harbor LaboratoriesUniversity of WashingtonFriday HarborUSA
  2. 2.Department of ZoologyArizona State UniversityTempeUSA

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