Effects of Axonal Topology on the Somatic Modulation of Synaptic Outputs

Abstract

Depolarization of the neuronal soma augments synaptic output onto postsynaptic neurons via long-range, axonal cable properties. Here, we report that the range of this somatic influence is spatially restricted by not only axonal path length but also a branching-dependent decrease in axon diameter. Cell-attached recordings of action potentials (APs) from multiple axon branches of a rat hippocampal CA3 pyramidal cell revealed that an AP was broadened following a 20 mV depolarization of the soma and reverted to a normal width during propagation down the axon. The narrowing of the AP depended on the distance traveled by the AP and on the number of axon branch points through which the AP passed. These findings were confirmed by optical imaging of AP-induced calcium elevations in presynaptic boutons, suggesting that the somatic membrane potential modifies synaptic outputs near the soma but not long-projection outputs. Consistent with this prediction, whole-cell recordings from synaptically connected neurons revealed that depolarization of presynaptic CA3 pyramidal cells facilitated synaptic transmission to nearby CA3 pyramidal cells, but not to distant pyramidal cells in CA3 or CA1. Therefore, axonal geometry enables the differential modulation of synaptic output depending on target location.

Na+ current in presynaptic terminals of the crayfish opener cannot initiate action potentials

“…The shape of on-cell transients ( Fig. 1A2) represents a combination of inversion and the time derivative of intracellular counterparts (Sasaki et al 2012). Whole cell access to the terminal, with a holding potential of Ϫ80 mV, gave rise to a holding current of Ϫ250 pA.…”

Modulation of spike-evoked synaptic transmission: The role of presynaptic calcium and potassium channels

“…Hybrid analog-digital enhancement of synaptic transmission at spiking synapses initially described in invertebrates [29,37,39,40] has been more recently reported in many mammalian synapses of the CNS including cortical [24,42,48], cerebellar [9,12], and hippocampal excitatory synapses ( [1,18,34]; Bialowas et al, 2014). In these examples, synaptic transmission evoked by single APs is enhanced as the result of analog-mediated depolarization (10-30 mV) of the presynaptic element for a few tens to hundreds of milliseconds (Fig.…”

“…In L5 pyramidal neurons, ADF is observed after several seconds of presynaptic depolarization [24,42] whereas a few tens of milliseconds of analog subthreshold depolarization is sufficient to induce ADF at mossy fiber-CA3 cell synapses [1] or at cerebellar GABAergic synapses [9]. At CA3-CA3 connections, the temporal requirement of ADF is not clear [34].…”

Multitasking in Gonadotropin-Releasing Hormone Neuron Dendrites

“…We therefore investigated the possibility that subthreshold synaptic inputs may modify the shape of action potentials as they propagate along the dendron. Previous studies in hippocampal neurons have demonstrated that subthreshold depolarizations in the axon can broaden action potentials leading to changes in neurotransmitter release [32,33,34,35]. To investigate whether this occurs in GnRH dendrons, we focally uncaged glutamate while recording dendritic spikes with an on-cell recording electrode.…”

“…It is important to note however that this effect on the shape of the spike will only be localized to the region of the dendron where the synaptic input occurs. At regions further down the projection, where the depolarization will be very small or negligible, the impact on spike shape will cease to exist [33]. Therefore, current evidence suggests that synaptic inputs onto this central region will not impact excitability either at the spike initiation site or the nerve terminals.…”