Local communication within dendritic spines: Models of second messenger diffusion in granule cell spines of the mammalian olfactory bulb

Abstract

Dendritic spines are generally believed to play a role in modulating synaptically induced electrical events. In addition, they may also confine second messengers and thus topologically limit the distance over which second messenger cascades may be functionally significant. In order to address this possibility, computer simulations of transient second messenger concentration changes were performed. The results show the importance of spine morphology and binding and extrusion mechanisms in controlling second messenger transients. In the presence of intrinsic cytoplasmic binding sites and kinetic rates similar to that expected for calcium, second messengers were confined to the spine head. In the absence of binding/extrusion mechanisms, the size and time course of the input transient to the spine head influenced the second messenger transients that might be seen at the base of the spine neck and in other spines. Large and/or sustained increases in second messenger concentration in the spine head were communicated to the spine base and to other spine heads. The results emphasize the importance of a knowledge of breakdown pathways, concentrations and kinetics of binding sites, and extrusion mechanisms for understanding the dynamics of local chemical changes for dendritic spine function.

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

“…Thus, the LTS represents a putative "presynaptic" signal that we propose to underlie AP-independent lateral inhibition between M/TCs. We saw no evidence for the regionally localized Ca 2ϩ signals described in some cell types (Eilers et al, 1995;Schiller et al, 1997;Wei et al, 2001) and proposed for GCs on theoretical grounds (Woolf et al, 1991a;Woolf and Greer, 1994); in our experiments, LTS-mediated lateral inhibition was never spatially restricted to subregions of the GC dendrite. However, regional LTS signals might be produced under different conditions, for example, shunting by ongoing synaptic input to GCs (Koch et al, 1982), different in vivo activation patterns, modulation by centrifugal input, or developmental changes of network properties.…”

“…However, although regional subthreshold signaling has been long suggested in GCs as a substrate for local lateral inhibition (Woolf et al, 1991b;Woolf and Greer, 1994;Isaacson and Strowbridge, 1998), we never observed the calcium spike signal (⌬F/F ) LTS to be restricted to a small dendritic region or dendritic branch only, in contrast to other low-threshold Ca 2ϩ spikes (Eilers et al, 1995;Wei et al, 2001). Instead, like the sAP-evoked calcium transients Egger et al, 2003), (⌬F/F ) LTS appeared throughout all areas of the dendritic tree of examined GCs, indicating that it was global in nature (Fig.…”

“…It has been hypothesized that this signal could be restricted to a local dendritic region (Woolf et al, 1991b;Woolf and Greer, 1994;Isaacson and Strowbridge, 1998). Such "dendritic subunits" have also been predicted based on compartmental models of other cell types (Koch et al, 1982;Shepherd and Brayton, 1987;Mel, 1993) and recently demonstrated in pyramidal cells (Polsky et al, 2004).…”

Three-Dimensional Organization of Smooth Endoplasmic Reticulum in Hippocampal CA1 Dendrites and Dendritic Spines of the Immature and Mature Rat

“…These results show that calcium is compartmentalized in CA1 spine heads after synaptic activation. The peak calcium occurring in a particular spine head will be sensitive to spine dimensions, cytoplasmic buffering, and the modulation of calcium via release from the SER, via sequestration into the SER, or from extrusion, via the Na ϩ /Ca 2ϩ exchange on the plasma membrane (Holmes and Levy, 1990;Zador et al, 1990;Gold and Bear, 1994;Woolf and Greer, 1994).…”

Calcium Entry through Cyclic Nucleotide-Gated Channels in Individual Cilia of Olfactory Receptor Cells: Spatiotemporal Dynamics

“…Collectively, the data of Figures 4 and 8 suggest that olfactory cilia function, at least to some extent, as discrete biochemical compartments with Ca 2ϩ dynamics that are relatively independent from those in the rest of the neuron, a situation not unlike that in other small neuronal compartments such as dendritic spines (cf. Woolf and Greer, 1994;Shepherd, 1996).…”