Trends in Neurosciences
Volume 21, Issue 11, 1 November 1998, Pages 453-460
Journal home page for Trends in Neurosciences

Perspective
Excitable dendrites and spines: earlier theoretical insights elucidate recent direct observations

https://doi.org/10.1016/S0166-2236(98)01327-7Get rights and content

Abstract

Important advances in experimental methods have made it possible to measure the electrical events in dendrites directly and to record optically from dendritic spines. These new techniques allow us to focus on the input region of the neuron and highlight the excitable properties of the dendritic membrane. Interestingly, some of the recent experimental findings were anticipated by earlier theoretical research, for example, the observation that some spines possess excitable channels that might generate local all-or-none events. Computer models were used previously to explore the conditions for initiating an action potential at the dendritic tree, in particular, at the spine head, and for active propagation between excitable spines and excitable dendritic arbors. The consequences for synaptic amplification, for the extent of active spread in the tree and for non-linear discriminations between different patterns of synaptic inputs were also considered. Here we review the biophysical insights gained from the theory and demonstrate how these elucidate the recent experimental results.

Trends Neurosci. (1998) 21, 453–460

Section snippets

A brief history of neuron modeling

Neurons are biological cells with highly developed properties of excitation and inhibition that depend upon rapid changes in cell-membrane permeability to certain ions in a way that was systematically elucidated by Hodgkin, Huxley and Katz during the period 1948–1952. They showed that excitation involves a very large increase in membrane permeability to Na+ ions, and that the resting state depends on a low permeability to Na+ ions and a relatively high permeability to K+ ions. Synaptic

Early dendritic models not restricted to passive membrane

The earliest modeling of dendrites began with the assumption that they had uniform passive membrane properties. However, several early papers included non-uniform membranes that contained regions with (1) different values for the specific membrane resistivity (Rm) (Ref. [31]), (2) non-linear efficacy of synaptic inhibitory conductance[32]and also, (3) excitable membrane[48]. The non-linear properties of synaptic interactions in dendritic trees were demonstrated and discussed, and a

Mitral and granule cell populations in olfactory bulb

Excitable dendritic membranes were explicitly included in the computations of Rall and Shepherd[48]. Here, the task was to model and compute extracellular field potentials that matched those observed experimentally in olfactory bulb when the mitral cell population was activated in near synchrony by means of an antidromic volley. A nine-compartment model (three axonal, one somatic and five dendritic) was used to simulate antidromic activation of a mitral cell, while a ten-compartment model was

Models of excitable dendritic spines

Increasing evidence that the dendrites of many neuron types are equipped with excitable channels raised the interesting possibility that spine membrane (which, depending on neuron type, occupies 20–70% of the total dendritic membrane) also bears excitable channels. The implication of excitable channels in the spine head membrane for amplification of excitatory synaptic inputs was first discussed rigorously by Jack[43]. Transient computations for excitable spines and exploration of conditions

Insights from theoretical models of excitable dendrites and spines

The key insights that were gained from these theoretical studies, which are directly relevant to the recent experimental findings, are summarized as follows: (1) In an excitable dendritic tree with uniform ion channel densities, the propagation of the AP is more secure towards distal branches; it is usually blocked proximally. In the distal direction (from soma to dendrites), the AP typically propagates from thicker to thinner branches, and towards the favorable (sealed-end) boundary conditions

Theory illuminates recent experimental results

The new IR-DIC video microscopy clearly demonstrates that dendrites of various cell types are endowed with a variety of excitable channels, including voltage-gated K+ and Na+ channels and various Ca2+ channel subtypes (Fig. 1A and Refs 11, 14, 17, 26, 28). Simultaneous recordings from the soma and dendrites show that the AP usually starts near the soma, probably in the axon beyond the initial segment[83], and then propagates actively backward into the dendrites (review in Ref. [16], see also

Concluding remarks

During the past few years, dendrites have become the focus of very detailed investigations. Within a short period of time many of the characteristics hidden in their membranes and concealed within their dendritic spines, have become experimentally accessible. The fascinating picture that has emerged shows that the dendritic tree is covered non-uniformly with a variety of excitable synaptic channels, each capable of operating on a different time scale and with activity-dependent sensitivity11, 14

Acknowledgements

This work was supported by grants from the ONR and the Israeli Academy of Science. We thank M. Rapp, S. Redman and A. Thomson for their critical reviews of the article.

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