Dendritic Sodium Spikelets and Low-Threshold Calcium Spikes in Turtle Olfactory Bulb Granule Cells

Abstract

Active dendritic membrane properties were investigated by whole cell recordings from adult turtle olfactory bulb granule cells. The laminar structure of the olfactory bulb allowed differential polarization of the distal apical dendrites versus the somatic part of the cells by an external electric field. Dendritic depolarization evoked small (∼10 mV) all-or-none depolarizing events of ∼10-ms duration. These spikelets often occurred in bursts at high frequency (≤250 Hz); they were present despite the application of synaptic and gap junction antagonists, but were abolished by TTX and intracellularly applied QX314. The spikelets were interpreted as attenuated sodium spikes initiated in different branches of the granule cells dendrites. They occurred spontaneously, but could also be evoked by excitatory postsynaptic potentials (EPSPs) to the distal dendrites. Spikelets initiated by distal excitation could function as prepotentials for full sodium spikes, in part depending on the level of proximal depolarization. Somatic depolarization by the electric field evoked full sodium spikes as well as low-threshold calcium spikes (LTSs). Calcium imaging revealed that the electrophysiologically identified LTS evoked from the soma was associated with calcium transients in the proximal and the distal dendrites. Our data suggest that the LTS in the soma/proximal dendrites plays a major role in boosting excitability, thus contributing to the initiation of sodium spiking in this compartment. The results furthermore suggest that the LTS and the sodium spikes may act independently or cooperatively to regulate dendritic calcium influx.

Dendrodendritic Synaptic Signals in Olfactory Bulb Granule Cells: Local Spine Boost and Global Low-Threshold Spike

“…Like APevoked Ca 2ϩ signals (Egger et al, 2003), the LTS was all-or-none in nature. The LTS signal was of a similar magnitude to APevoked Ca 2ϩ signals, and, like the AP-evoked signal, the LTS spread globally throughout the dendrites, similar to observations in turtle olfactory bulb GCs by Pinato and Midtgaard (2004). Thus, the LTS represents a putative "presynaptic" signal that we propose to underlie AP-independent lateral inhibition between M/TCs.…”

“…Yet another type of regional Ca 2ϩ signal, perhaps attributable to spatially restricted Na ϩ spikes (spikelets) (Wellis and Scott, 1990;Luo and Katz, 2001;Pinato and Midtgaard, 2004), has been observed in frog olfactory bulb GC dendrites (K. Delaney, personal communication).…”

Branch-Specific Ca2+Influx from Na+-Dependent Dendritic Spikes in Olfactory Granule Cells

“…Activation of excitatory synaptic inputs by stimulation of mitral cells causes a mixed response in granule cells comprised of synaptic potentials, D-spikes, and sometimes SAPs. Similar dendritically generated spikes with a significant Na ϩ dependence have been reported recently in response to evoked synaptic excitation in isolated turtle olfactory bulb (Pinato and Midtgaard, 2005). Ca 2ϩ imaging experiments are described in following sections to directly support the conclusion that, although they are subthreshold in the soma, these events correspond to large amplitude suprathreshold action potentials in the dendrites.…”

“…Additionally, we find that primarily Na ϩ -dependent, dendritic spikes (D-spikes) produce Ca 2ϩ transients that can be restricted to subsets of dendritic branches. This adds to growing evidence for dendritically generated active events in granule cells of turtle and rat reported recently by Pinato and Midtgaard (2005) and Egger et al (2005). In frog, the soma and proximal dendritic segment appear to be a barrier to their propagation, resulting in restriction of D-spikeevoked Ca 2ϩ influx to sets of spines on peripheral branches.…”

Electrogenesis in the lower Metazoa and implications for neuronal integration

“…The difference in threshold allows the Ca 2+ spike to propagate independently, below the threshold for escape swimming. Although apparently unique in the invertebrate kingdom, these low-amplitude Ca 2+ spikes resemble those recorded from dendritic fields in the vertebrate brain (Llinás and Yarom, 1981;Pinato and Midtgaard, 2005). …”