Skip to main content
Log in

In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia

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

Abstract

  1. 1.

    We are studying the neural basis of consummatory feeding behavior in Aplysia using intact, freely moving animals.

  2. 2.

    Video records show that the timing of radula closure during the radula protraction-retraction cycle constitutes a major difference between ingestion (biting or swallowing) and rejection. During ingestion, the radula is closed as it retracts. During rejection, the radula is closed as it protracts.

  3. 3.

    We observed two patterns of activity in nerves which are likely to mediate these radula movements. Patterns I and II are associated with ingestion and rejection, respectively, and are distinguished by the timing of radula nerve activity with respect to the onset of buccal nerve 2 activity.

  4. 4.

    The association of ingestion with pattern I is maintained when the animal feeds on a polyethylene tube, the same food substrate used to elicit rejection responses. Under these conditions, pattern I is associated with either swallowing or no net tube movement.

  5. 5.

    Most transitions from swallowing to rejection were preceded by one or more occurrences of pattern I in which there was no net tube movement, suggesting that these transitions can be predicted.

  6. 6.

    Our data suggest that these two patterns can be used to distinguish ingestion from rejection.

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.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BN2:

buccal nerve 2

RN:

radula nerve

References

  • Audesirk TE, Audesirk GJ (1979) Oral mechanoreceptors in Tritonia diomedea. II. Role in feeding. J Comp Physiol 130:79–86

    Google Scholar 

  • Chiel HJ, Weiss KR, Kupfermann I (1986) An identified histaminergic neuron modulates feeding motor circuitry in Aplysia. J Neurosci 6:2427–2450

    Google Scholar 

  • Church PJ, Lloyd PE (1991) Expression of diverse neuropeptide cotransmitters by identified motor neurons in Aplysia. J Neurosci 11:618–625

    Google Scholar 

  • Church PJ, Cohen KP, Scott ML, Kirk MD (1991) Peptidergic motoneurons in the buccal ganglia of Aplysia californica: Immunocytochemical, morphological, and physiological characterizations. J Comp Physiol A 168:323–336

    Google Scholar 

  • Cohen JL, Weiss KR, Kupfermann I (1978) Motor control of buccal muscles in Aplysia. J Neurophysiol 41:157–180

    Google Scholar 

  • Croll RP, Davis WJ (1981) Motor program switching in Pleurobranchaea. I. Behavioural and electromyographic study of ingestion and egestion in intact specimens. J Comp Physiol 145:277–287

    Google Scholar 

  • Croll RP, Davis WJ, Kovac MP (1985a) Neural mechanisms of motor program switching in the mollusc Pleurobranchaea. I. Central motor programs underlying ingestion, egestion, and the “neutral” rhythm(s). J Neurosci 5:48–55

    Google Scholar 

  • Croll RP, Kovac MP, Davis WJ (1985b) Neural mechanisms of motor program switching in the mollusc Pleurobranchaea. II. Role of the ventral white cell, anterior ventral, and B3 buccal neurons. J Neurosci 5:56–63

    Google Scholar 

  • Croll RP, Kovac MP, Davis WJ, Matera EM (1985c) Neural mechanisms of motor program switching in the mollusc Pleurobranchaea. III. Role of paracerebral neurons and other identified brain neurons. J Neurosci 5:64–71

    Google Scholar 

  • Cropper EC, Kupfermann I, Weiss KR (1990) Differential firing patterns of the peptide-containing cholinergic motor neurons B15 and B16 during feeding behavior in Aplysia. Brain Res 522:176–179

    Google Scholar 

  • Fiore L, Meunier J-M (1979) Synaptic connections and functional organization in Aplysia buccal ganglia. J Neurobiol 10:13–29

    Google Scholar 

  • Gardner D (1971) Synaptic organization and bilateral symmetry in the buccal ganglia of Aplysia. Ph. D. Thesis, New York University

  • Gelperin A, Chang JJ, Reingold SC (1978) Feeding motor program in Limax. I. Neuromuscular correlates and control by chemosensory input. J Neurobiol 9:285–300

    Google Scholar 

  • Harnett DL (1975) Introduction to statistical methods. Addison-Wesley, Reading, pp 521–524

    Google Scholar 

  • Heinzel HG (1988a) Gastric mill activity in the lobster. I. Spontaneous modes of chewing. J Neurophysiol 59:528–550

    Google Scholar 

  • Heinzel HG (1988b) Gastric mill activity in the lobster. II. Proctolin and octopamine initiate and modulate chewing. J Neurophysiol 59:551–565

    Google Scholar 

  • Heinzel HG, Selverston AI (1988) Gastric mill activity in the lobster. III. Effects of proctolin on the isolated central pattern generator. J Neurophysiol 59:566–585

    Google Scholar 

  • Hooper SL, Moulins M (1989) Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244:1587–1589

    Google Scholar 

  • Hurwitz I, Susswein AJ (1992) Adaptation of feeding sequences in Aplysia oculifera of changes in the load and width of food. J Exp Biol 166:215–235

    Google Scholar 

  • Kandel ER (1979) Behavioral biology of Aplysia. Freeman, San Francisco

    Google Scholar 

  • Kater SB (1974) Feeding in Helisoma trivolvis: The morphological and physiological bases of a fixed action pattern. Am Zool 14:1017–1036

    Google Scholar 

  • Kupfermann I (1974) Feeding behavior in Aplysia: A simple system for the study of motivation. Behav Biol 10:1–26

    Google Scholar 

  • Lloyd PE (1988) Fast axonal transport of modulatory neuropeptides from central ganglia to components of the feeding system in Aplysia. J Neurosci 8:3507–3514

    Google Scholar 

  • McClellan AD (1982a) Movements and motor patterns of the buccal mass of Pleurobranchaea during feeding, regurgitation, and rejection. J Exp Biol 98:195–211

    Google Scholar 

  • McClellan AD (1982b) Re-examination of presumed feeding motor activity in the isolated nervous system of Pleurobranchaea. J Exp Biol 98:213–228

    Google Scholar 

  • Morton DW, Chiel HJ (1991) Two patterns of buccal nerve activity that distinguish ingestion from rejection can be replicated in a reduced preparation in Aplysia. Soc Neurosci Abstr 17:1593

    Google Scholar 

  • Morton DW, Chiel HJ, Cohen LB, Wu J-Y (1991) Optical methods can be utilized to map the location and activity of putative motor neurons and interneurons during rhythmic patterns of activity in the buccal ganglion of Aplysia. Brain Res 564:45–55

    Google Scholar 

  • Nagahama T, Takata M (1988) Food-induced firing patterns in motoneurons producing jaw movements in Aplysia kurodai. J Comp Physiol A 162:729–738

    Google Scholar 

  • Plumb GO (1965) Pulse height analyser for electrophysiology. J Physiol (Lond) 179:16P-17P

    Google Scholar 

  • Plummer MR, Kirk MD (1990) Premotor neurons B51 and B52 in the buccal ganglia of Aplysia californica: Synaptic connections, effects on ongoing motor rhythms, and peptide modulation. J Neurophysiol 63:539–558

    Google Scholar 

  • Rose RM (1971) Patterned activity of the buccal ganglion of the nudibranch mollusc Archidoris pseudoargus. J Exp Biol 55:185–204

    Google Scholar 

  • Rose RM (1972) Burst activity of the buccal ganglion of Aplysia depilans. J Exp Biol 56:735–754

    Google Scholar 

  • Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80:137–163

    Google Scholar 

  • Rosen SC, Teyke T, Miller MW, Weiss KR, Kupfermann I (1991) Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J Neurosci 11:3630–3655

    Google Scholar 

  • Scott ML, Govind CK, Kirk MD (1991) Neuromuscular organization of the buccal system in Aplysia californica. J Comp Neurol 312:207–222

    Google Scholar 

  • Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Sossin WS, Kirk MD, Scheller RH (1987) Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia. J Neurosci 7:671–681

    Google Scholar 

  • Susswein AJ, Byrne JH (1988) Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia. 3 J. Neurosci 8:2049–2061

    Google Scholar 

  • Susswein AJ, Kupfermann I, Weiss KR (1976) The stimulus control of biting in Aplysia. J Comp Physiol 108:75–96

    Google Scholar 

  • Weimann JM, Meyrand P, Marder E (1991) Neurons that form multiple pattern generators: Identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J Neurophysiol 65:111–122

    Google Scholar 

  • Weiss KR, Chiel HJ, Koch U, Kupfermann I (1986) Activity of an identified histaminergic neuron, and its possible role in arousal of feeding behavior in semi-intact Aplysia. J Neurosci 6:2403–2415

    Google Scholar 

  • Willows AOD (1980) Physiological basis of feeding behavior in Tritonia diomedea. II. Neuronal mechanisms. J Neurophysiol 44:849–861

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morton, D.W., Chiel, H.J. In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia . J Comp Physiol A 172, 17–32 (1993). https://doi.org/10.1007/BF00214712

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214712

Key words

Navigation