Extrinsic modulation and motor pattern generation in a feeding network: a cellular study

Systems level studies have shown that the paired serotonergic cerebral gian t cells (CGCs) of gastropod mollusks have important extrinsic modulatory ac tions on the central pattern generator (CPG) underlying rhythmic ingestion movements. Here we present the first study that investigates the modulatory actions of the CGCs and their released transmitter 5-HT on the CPG at the cellular level. In the snail, Lymnaea, motoneurons such as the B4, B8, and B4CL cells are part of the feeding CPG and receive serotonergic synaptic in puts from CGCs. These motoneurons were used to investigate the effect of se rotonergic modulation on endogenous cellular properties of CPG neurons. Cel ls were isolated from the intact nervous system, and their properties were examined by pharmacological methods in cell culture. Motoneurons were also grown in coculture with CGCs to compare 5-HT effects with CGC stimulation. Three distinct modulatory effects of exogenously applied 5-HT/CGC activity were seen: all three motoneuron types were depolarized by 5-HT for prolonge d periods leading to firing. Conditional bursting accompanied this depolari zation in the B4/B8 cells, but not in B4CL cells. The frequency of the burs ting was increased with increased CGC tonic firing. An increase in the size of postinhibitory rebound (PIR) occurred with 5-HT application in all thre e cell types, because of an increase in a CsCl-sensitive, hyperpolarization -activated inward current. Similar modulatory effects on membrane potential , endogenous bursting, and PIR properties could be observed in the intact n ervous system and were necessary for motoneuron activation during feeding. Part of the systems gating and frequency control functions of the CGCs appe ar to be caused by these modulatory effects on feeding motoneurons.