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Comparative neuroethology of feeding control in molluscs

C. J. H. Elliott^1,* and A. J. Susswein²

¹ Department of Biology, University of York, York YO10 5YW, UK
² Faculty of Life Sciences, Gonda (Goldschmied) Medical Diagnostic Research Center, Bar-Ilan University, Ramat-Gan 52 900, Israel

View larger version (25K): [in a new window]   Fig. 1. The herbivorous gastropods studied include the marine opisthobranchs Aplysia (10 cm long) and Pleurobranchaea (5 cm long, eating a nudibranch, Flabellina which is coloured purple and orange) and the pulmonates Helix (terrestrial, 2 cm long) and three freshwater genera (Planorbis, Helisoma and Lymnaea, all 1 cm long). The pictures are not to scale. We are grateful to Rhanor Gillette and Andy Bulloch for the pictures of Pleurobranchaea and Helisoma.

View larger version (30K): [in a new window]   Fig. 2. Feeding movements of (A) Lymnaea and (B) Aplysia. (A) Schematic diagram of the feeding sequence of Lymnaea in which the three phases of movement (protraction, rasp and swallow) are shown diagrammatically. The muscles of the buccal mass — principally the anterior and posterior jugalis (aj, pj) and radular tensor (rt) — contract, squeezing and rotating the odontophore (OD). This is covered by the many-toothed radula (R), which is rasped across the substratum. Food particles are then collected and passed into the oesophagus (OE). M, mouth. After Benjamin and Elliott (1989). (B) A biting sequence in Aplysia. The food that elicited the movement is not shown. (i) The animal is in the head-up feeding position. (ii) The animal moves its head and lips to centre the food close to the mouth. (iii) The mouth opens, and the radula protracts forward out of the mouth. Note that the radula halves are open during the protraction. (iv-vi) The radula gradually retracts and the mouth closes. Note that the radula halves close. Closure coupled with the retraction pulls the food into the mouth. After Kupfermann (1974).

View larger version (30K): [in a new window]   Fig. 3. Neuronal circuits contributing to feeding in (A) Lymnaea and (B) Aplysia. (A) The main monosynaptic neuronal connections within the feeding system of Lymnaea in the three phases of feeding. In each phase, the same set of interneurones, motoneurones and buccal mass muscles are indicated, with active neurones and muscles shown filled. The main chemical outputs of the active neurones are shown, with some connections shown as dotted lines to aid clarity. CGC and CV are cerebral neurones, SO, N1M, N2v, N3t and OC are interneurones in the buccal ganglia. B1-B4, B6, B7 and B10 are motoneurones in the buccal ganglia that innervate the salivary gland (sg) oesophagus (oe), an oesophageal gland (og), the anterior and posterior jugalis muscles (aj, pj) and the radular tensor muscle (rt). Rhythmic cycling of the feeding network arises from the synaptic connections, with a major role for biphasic connections, and the timing of the network is controlled by endogenous properties of the cells, e.g. endogenous bursting or plateau potentials. (B) The main synaptic pathways in the neuronal network for feeding in Aplysia. All the connections shown are monosynaptic except for the connection from C-PR to MCC and the CBIs, which go through interneurones in the pleural ganglion. The CBIs and MCC also receive inputs from the central pattern generator, but the synaptic details of this have not been published. The C2, MCC, CBI and C-PR neurones and the lip sensory neurones are in the cerebral ganglia, the other neurones in the buccal ganglia. The B63-B31/B32 interneurones control protraction; B51 and B64 control retraction. The relative activities of B51, B34 and B21 control whether the pattern leads to ingestion or egestion. Note that some neurones, such as B51, have multiple roles. The population of sensory neurones includes both chemosensory and mechanosensory cells.

View larger version (28K): [in a new window]   Fig. 4. (A) Consistency among the gastropods in the occurrence of protraction-phase interneurones with axons ascending in the contralateral cerebro-buccal connective. Planorbis group 1 interneurone (Arshavsky et al., 1988a); Lymnaea N1 interneurone (Elliott and Benjamin, 1985a); Aplysia B34 interneurone (Hurwitz et al., 1997). (B) Variation between retraction-phase (N3) neurones in Lymnaea. The anatomical variation shown is accompanied by physiological and pharmacological variation: the tonic N3 fires many action potentials, each producing a short excitatory postsynaptic potential on the B3 motoneurone, while the phasic N3 and OC cells fire transiently at the start of this phase. The phasic N3 neurone produces a long-lasting excitation of N3 and the OC an inhibition of the B3 motoneurone. The OC (but not the other interneurones) uses octopamine as its transmitter. Modified from Elliott and Benjamin (1985a) and Vehovszky et al. (1998).

View larger version (29K): [in a new window]   Fig. 5. Conditioning Helix to carrot or potato changes the responses recorded in the peritentacular nerves in an isolated tentacle/ganglion preparation. Snails were presented with either carrot (i) or potato (ii) and allowed to feed. (A) Naïve snails; (B) carrot-conditioned snails; (C) potato-conditioned snails. The extracellular recordings of nerve activity show increased activity when the odour of their food was blown across the tentacle. Reproduced from Peschel et al. (1996) with permission.