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 Ca(2+) 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.

Graded boosting of synaptic signals by low-threshold voltage-activated calcium conductance

“…The activation of this NNC-sensitive Ca 2ϩ signal is a graded function of the amplitude of the synaptic response (Yang et al 2013), which is coherent with the graded amplification shown in Fig. 2.…”

“…Background fluorescence was measured in an equivalent region of the focal plane, away from the cell recorded from. Changes in fluorescence that resulted from bleaching were negligible at the moment of stimulation and needed no correction for analyzing the Ca 2ϩ signals (Yang et al 2013).…”

“…It has been shown that synaptically evoked responses cause an increase in the [Ca 2ϩ ] i of NS neurons for which magnitude is a linear function of the amplitude of ⌬V m NS and that these Ca 2ϩ signals exhibit a relatively constant magnitude along the neuronal branches (Yang et al 2013). These data were interpreted as an indication that the LT-VACC is distributed throughout NS branches.…”

“…Among these conductances, low-threshold voltage-activated calcium conductances (LT-VACCs) play a substantial role in shaping the biophysical attributes of neurites (Huguenard 1996), suggesting their involvement in synaptic processing. Synaptic stimulation or focal subthreshold depolarization activate calcium conductances in the dendritic arbor of a variety of neurons (Egger et al 2005;Eilers et al 1995;Errington et al 2010;Ivanov and Calabrese 2006;Laurent et al 1993;Schiller et al 1997;Wessel et al 1999;Yang et al 2013;Yuste and Denk 1995). However, it is not known to what extent the activation of LT-VACCs shapes the synaptic responses that gave rise to them, influencing their magnitude, dynamics, and propagation.…”

“…Calcium imaging studies have shown that this LT-VACC is distributed throughout the main branches and is activated by synaptic responses evoked by stimulation of pressure-sensitive (P) neurons (Yang et al 2013). The resulting Ca 2ϩ signals are a graded function of the electrophysiological synaptic responses and spread throughout the neuritic tree with no major attenuation.…”