Spatial segregation of excitatory and inhibitory effects of 5-HT on crayfish motoneurons

Abstract

Altering neuronal membrane properties, including input resistance, is a key modulatory mechanism for changing neural activity patterns. The effect of membrane currents generated by either synaptic or voltage-dependent channels directly depends on neuron input resistance. We found that local application of serotonin to different regions of identified motoneurons (MNs) of the postural/walking network of isolated crayfish produced different changes in input resistance. Puff-applied 5-HT in the periphery of the initial segment produced exclusively inhibitory responses. In contrast, when 5-HT was puff-applied on the central arbor of the same depressor (Dep) MN, exclusively depolarizing responses were obtained. Both inhibitory and excitatory responses were direct because they persisted in low-calcium saline. We found numerous close appositions between 5-HT-immunoreactive processes and the initial segment of dextran-rhodamine-filled Dep MNs. In contrast, almost no close apposition sites were found in Dep MN arbor. It seems that the 5-HT controls the level of excitability of postural network MNs by two mechanisms acting at two different sites: inhibitory responses (consistent with an action involving opening of K+ channels) occur in the initial segment region and may involve classic synaptic transmission, whereas depolarizing responses (consistent with an action involving closing of K+ channels) occur on MN branches via apparent paracrine effects.