Coding and Decoding with Adapting Neurons: A Population Approach to the Peri-Stimulus Time Histogram

The response of a neuron to a time-dependent stimulus, as measured in a Peri-Stimulus-Time-Histogram (PSTH), exhibits an intricate temporal structure that reflects potential temporal coding principles. Here we analyze the encoding and decoding of PSTHs for spiking neurons with arbitrary refractoriness and adaptation. As a modeling framework, we use the spike response model, also known as the generalized linear neuron model. Because of refractoriness, the effect of the most recent spike on the spiking probability a few milliseconds later is very strong. The influence of the last spike needs therefore to be described with high precision, while the rest of the neuronal spiking history merely introduces an average self-inhibition or adaptation that depends on the expected number of past spikes but not on the exact spike timings. Based on these insights, we derive a ‘quasi-renewal equation’ which is shown to yield an excellent description of the firing rate of adapting neurons. We explore the domain of validity of the quasi-renewal equation and compare it with other rate equations for populations of spiking neurons. The problem of decoding the stimulus from the population response (or PSTH) is addressed analogously. We find that for small levels of activity and weak adaptation, a simple accumulator of the past activity is sufficient to decode the original input, but when refractory effects become large decoding becomes a non-linear function of the past activity. The results presented here can be applied to the mean-field analysis of coupled neuron networks, but also to arbitrary point processes with negative self-interaction. Author Summary: How can information be encoded and decoded in populations of adapting neurons? A quantitative answer to this question requires a mathematical expression relating neuronal activity to the external stimulus, and, conversely, stimulus to neuronal activity. Although widely used equations and models exist for the special problem of relating external stimulus to the action potentials of a single neuron, the analogous problem of relating the external stimulus to the activity of a population has proven more difficult. There is a bothersome gap between the dynamics of single adapting neurons and the dynamics of populations. Moreover, if we ignore the single neurons and describe directly the population dynamics, we are faced with the ambiguity of the adapting neural code. The neural code of adapting populations is ambiguous because it is possible to observe a range of population activities in response to a given instantaneous input. Somehow the ambiguity is resolved by the knowledge of the population history, but how precisely? In this article we use approximation methods to provide mathematical expressions that describe the encoding and decoding of external stimuli in adapting populations. The theory presented here helps to bridge the gap between the dynamics of single neurons and that of populations.