Patterned Activity of the Buccal Ganglion of the Nudibranch Mollusc Archidoris Pseudoargus

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Abstract
In recent years there have been a number of analyses of patterned activity in invertebrate ganglia. Examples include the studies of crayfish swimmeret beat (Hughes & Wiersma, 1960), the flight system of insects (Weis-Fogh, 1964; Wilson, 1966; Wyman, 1966) and crustacean heart-beat control (Maynard, 1966). In the Mollusca, Horridge (1960) described the production of patterned discharges from the cerebral ganglia of the clam Mya by electrical stimulation of the cerebral nerves, and Turner (1966) described a similar type of response from the pedal ganglion of Agriolimax.More recently, Dorsett, Willows & Hoyle (1969) have described the production of a patterned sequence of bursts of impulses by a small group of symmetrically placed cells in the pedal ganglion of Tritonia gilberti during swimming. These swimming movements were elicited by contact with certain echinoderms, by liquid soap applied to the body surface, or by direct electrical stimulation of certain cells, although the sequence production could also be produced in the isolated brain by electrical stimulation of the cerebral nerves which supply the oral veil. Kandel, Frazier & Wachtel (1969) have also discussed the importance of inhibition in burst production by the abdominal ganglion of Aplysia californica.Until recently the only electrophysiological study of the buccal ganglion was that of Strumwasser (1967), who showed that synchronous bursts were produced in the buccal ganglion of Aplysia californica as a result of common synaptic input to symmetrically placed cells. This work has been extended by Gardner (1969), who described both common input and the presence of a single interneurone with input to six cells in the ipselateral ganglion. Levitan, Segundo & Tauc (1970), in another study on the ophistobranch Navanax inermis, have described electrical connexions between ten identifiable cells and have given a quantitative description of the coupling coefficients between these cells.The buccal mass of molluscs has been the subject of many investigations from the point of view of functional morphology (Fretter & Graham, 1962; Nisbet, 1954), but there have been no electrophysiological interpretations of radula movements. In the present study a natural stimulus has been used to induce feeding movements in the isolated buccal mass, and extracellular recording methods have been used to show that the buccal ganglion produces a sequence of bursts during radula movement. An account of the structure and nerve supply of the buccal mass of A. pseudoargus has been given elsewhere (Rose, 1970).The induction procedure involved first starving the animal, then isolating the buccal mass, and finally presenting the sponge (on which the animal normally feeds) to the isolated buccal mass. This frequently had the effect of inducing radula movements similar to those of normal feeding.Animals were isolated in separate aquarium tanks and starved for 3–4 days prior to the experiment. Isolation was necessary, since animals which were reproducing usually gave poor induction responses. The animals usually fed for periods of 15–20 h, but animals which were feeding also gave poor responses. Starvation for 3 or 4 days seemed to provide optimum conditions. Just before the experiment the animal was presented with sponge as a check, since animals which went to the sponge immediately usually gave the best results.During the dissection the mantle was first removed from the anterior third of the animal, care being taken to prevent mucus from contacting the buccal mass. The connective tissue covering the brain was then dissected away and the buccal mass, brain, and buccal ganglia were removed from the animal. This was done by cutting through the oesophagus, the paired postero-lateral retractor muscles M11(Rose, 1970) and the muscles round the mouth, so that the dissected buccal mass was complete with oral tube and oral tentacles. The branchial, pedal, visceral and rhinophore nerves were cut, but great care was taken not to damage any of the twenty buccal and cerebral nerves supplying the buccal mass, as damage seriously affected the induced responses.The buccal mass was then pinned out under sea water, with the buccal ganglia uppermost, and a piece of fresh sponge was placed in the bath beside the buccal mass. It was very important that the sponge was fresh, since animals will not normally feed on sponge which is even partially decayed. The breadcrumb sponge, Halichondria panicea, was used throughout these experiments. Archidoris feeds on other sponges, particularly the red sponge, Hymeniacidon perleve (Thompson, 1966), but inferior responses were generally obtained when these were used. In some experiments wholeanimal preparations were attempted with the mantle partly removed and the rhinophore nerves left intact. There was little difference between the responses obtained from this nearly intact preparation and those obtained when the buccal mass was completely removed, so the isolated preparation was more frequently used since it was easier to make the recordings in this condition.The buccal mass was dissected out in the usual way, and under the experimental conditions described above. It was opened up by a dorsal longitudinal cut along the top of the oral tube and buccal mass as far as the oesophagus, to expose the radula. A needle threaded with cotton was pushed through the radula and underlying odontophore cartilage of one half of the radula, and tied in a loop. The odontophore formed a convenient anchor, as well as being the structure responsible for movement of the radula. The buccal mass was then pinned under sea water with several pins through be oesophagus posteriorly and one through the ventral wall of the outer constrictor muscle M 5 (Rose, 1969) anteriorly. The other end of the cotton thread was tied to a balanced lever, positioned in line with the radula movements, and radula movements were recorded using a phototransistor arrangement to...