Two distinct mechanisms mediate potentiating effects of depolarization on synaptic transmission

Two distinct mechanisms mediate potentiating effects of depolarization on synaptic transmission. Recently there has been renewed interest in a type of plasticity in which a neuron's somatic membrane potential influences synaptic transmission. We study mechanisms that mediate this type of control at a synapse between a mechanoafferent, B21, and B8, a motor neuron that receives chemical synaptic input. Previously we demonstrated that the somatic membrane potential determines spike propagation within B21. Namely, B21 must be centrally depolarized if spikes are to propagate to an output process. We now demonstrate that this will occur with central depolarizations that are only a few millivolts. Depolarizations of this magnitude are not, however, sufficient to induce synaptic transmission to B8. B21-induced postsynaptic potentials (PSPs) are only observed if B21 is centrally depolarized by >or=10 mV. Larger depolarizations have a second impact on B21. They induce graded changes in the baseline intracellular calcium concentration that are virtually essential for the induction of chemical synaptic transmission. During motor programs, subthreshold depolarizations that increase calcium concentrations are observed during one of the two antagonistic phases of rhythmic activity. Chemical synaptic transmission from B21 to B8 is, therefore, likely to occur in a phase-dependent manner. Other neurons that receive mechanoafferent input are electrically coupled to B21. Differential control of spike propagation and chemical synaptic transmission may, therefore, represent a mechanism that permits selective control of afferent transmission to different types of neurons contacted by B21. Afferent transmission to neurons receiving chemical synaptic input will be phase specific, whereas transmission to electrically coupled followers will be phase independent.