Computation in a single neuron: Hodgkin and Huxley revisited

A spiking neuron "computes" by transforming a complex dynamical input into a train of action potentials, or spikes. The computation performed by the neuron can be formulated as dimensional reduction, or feature detection, followed by a nonlinear decision function over the low-dimensional space. Generalizations of the reverse correlation technique with white noise input provide a numerical strategy for extracting the relevant low-dimensional features from experimental data, and information theory can be used to evaluate the quality of the low-dimensional approximation. We apply these methods to analyze the simplest biophysically realistic model neuron, the Hodgkin-Huxley (HH) model, using this system to illustrate the general methodological issues. We focus on the features in the stimulus that trigger a spike, explicitly eliminating the effects of interactions between spikes. One can approximate this triggering "feature space" as a two-dimensional linear subspace in the high-dimensional space of input histories, capturing in this way a substantial fraction of the mutual information between inputs and spike time. We find that an even better approximation, however, is to describe the relevant subspace as two dimensional but curved; in this way, we can capture 90% of the mutual information even at high time resolution. Our analysis provides a new understanding of the computational properties of the HH model. While it is common to approximate neural behavior as "integrate and fire," the HH model is not an integrator nor is it well described by a single threshold.