MODULATORY ROLE FOR THE SEROTONERGIC CEREBRAL GIANT-CELLS IN THE FEEDING SYSTEM OF THE SNAIL, LYMNAEA .1. FINE WIRE RECORDING IN THE INTACTANIMAL AND PHARMACOLOGY

1. The role of the paired serotonergic cerebral giant cells (CGCs) in the feeding system of Lymnaea was examined by electrophysiological and pharmacological techniques. 2. The firing characteristics of the CGCs were recorded by fine wires attached to their cell bodies in freely m oving intact snails (in vivo recording) and their ''physiological'' ra tes of firing determined during feeding and other behaviors. 3. The me an CGC firing rates recorded in vivo varied between 1 and 20 spikes/mi n but never reached the average rates seen in the isolated CNS (60-120 spikes/min). Maximum rates of firing were seen during bouts of radula biting/rasping movements characteristic of the consummatory phase of feeding (15 +/- 1.69 spikes/min, mean +/- SE, range 7-20 spikes/min), with lower rates seen during locomotion {6.7 +/- 0.75 spikes/min; rang e 5-9 spikes/ min. The cells were rarely active when the animal was qu iescent (1.45 +/- 0.91 spikes/min; range 0-2 spikes/min). 4. In vivo r ecorded CGC firing was phase locked to the feeding movements of the an imal, with spikes occurring just before the opening of the mouth, duri ng the protraction phase of the feeding cycle. 5. Evoking firing rates on the CGCs in the isolated preparation similar to those seen in vivo during rasping movements (7-20 spikes/min) did not elicit a fictive f eeding pattern in an inactive preparation. Neither did bath applicatio n of 10(-9) M serotonin (5-HT; the transmitter of the CGCs). 6. To all ow the modulatory role of the CGCs to be examined during patterned act ivity, the fictive feeding pattern was evoked in the isolated preparat ion by injecting depolarizing current into a modulatory neuron, the sl ow oscillator (SO). 7. The tonic firing activity of the CGCs was accur ately maintained by current injection in the isolated preparation at r ates equivalent to that occurring during feeding, locomotion, and quie scence in the intact snail. This was possible where the CGCs became si lent after 1-2 h. Only when the CGCs activity was maintained at a rate (similar to 15 spikes/min) similar to that occurring during rasping, was the SO able to drive a full, high-frequency fictive feeding patter n (15-20 cycles/min). At lower rates of CGC firing, the SO-driven rhyt hm was either of lower frequency or no rhythm occurred at all (CGCs si lent). 8. In many isolated preparations (80%) the CGCs remained active , and it was difficult to maintain specific levels of tonic activity b y current injection. Here attempts to completely suppress CGC activity produced a lowering of fictive feeding rates but did not lead to the complete loss of the SO-driven pattern in the isolated preparation. Re sidual levels of CGC activity (axon spikes recorded) were still likely to be present. 9. Low concentrations of 5-HT (10(-9)-10(-8) M) perfus ed over the buccal ganglia allowed the SO to drive a full, high-freque ncy fictive feeding rhythm in preparations where the CGCs were already silent or spike activity had been suppressed by hyperpolarizing curre nt injection. 10. Perfusion of a variety of serotonergic antagonists a cross the buccal ganglia [7-methyltryptamine (7-MT) and cinanserin], w hen the CGCs were tonically active, slowed the rate of the SO-driven m otor program to values comparable with mean frequencies seen in the CG C spike suppression experiments. 11. It is concluded that the CGCs and their transmitter 5-HT have a modulatory rather than a command functi on in the feeding system of Lymnaea. One type of modulation (gating fu nction) requires a sufficient level of activity in the CGCs to ''enabl e'' a second type of neuron (the SO) to drive a feeding rhythm. Above this gating threshold (7 spikes/min), within the 7-to 20-spikes/min fi ring range, the CGCs influence the frequency of the motor pattern, a s econd type of modulatory function.