Wide propagation of graded signals in nonspiking neurons

Abstract

Signal processing in neuritic trees is ruled by the concerted action of passive and active membrane properties that, together, determine the degree of electrical compartmentalization of these trees. We analyzed how active properties modulate spatial propagation of graded signals in a pair of nonspiking (NS) neurons of the leech. NS neurons present a very extensive neuritic tree that mediates the interaction with all the excitatory motoneurons in leech ganglia. NS cells express voltage-activated Ca2+conductances (VACCs) that, under certain experimental conditions, evoke low-threshold spikes. We studied the distribution of calcium transients in NS neurons loaded with fluorescent calcium probes in response to low-threshold spikes, electrical depolarizing pulses, and synaptic inputs. The three types of stimuli evoked calcium transients of similar characteristics in the four main branches of the neuron. The magnitude of the calcium transients evoked by electrical pulses was a graded function of the change in NS membrane potential and depended on the baseline potential level. The underlying VACCs were partially inactivated at rest and strongly inactivated at −20 mV. Stimulation of mechanosensory pressure cells evoked calcium transients in NS neurons whose amplitude was a linear function of the amplitude of the postsynaptic response. The results evidenced that VACCs aid an efficient propagation of graded signals, turning the vast neuritic tree of NS cells into an electrically compact structure.