Sensitivity of firing rate to input fluctuations depends on time scale separation between fast and slow variables in single neurons

Neuronal responses are often characterized by the firing rate as a function of the stimulus mean, or the f-I curve. We introduce a novel classification of neurons into Types A, B-, and B+ according to how f-I curves are modulated by input fluctuations. In Type A neurons, the f-I curves display little sensitivity to input fluctuations when the mean current is large. In contrast, Type B neurons display sensitivity to fluctuations throughout the entire range of input means. Type B- neurons do not fire repetitively for any constant input, whereas Type B+ neurons do. We show that Type B+ behavior results from a separation of time scales between a slow and fast variable. A voltage-dependent time constant for the recovery variable can facilitate sensitivity to input fluctuations. Type B+ firing rates can be approximated using a simple energy barrier model.