Control of neuronal discharge timing by afferent fiber number and the temporal pattern of afferent impulses

We employ computer simulations to explore the effect of different temporal patterns of afferent impulses on the evoked discharge of a model cerebellar Purkinje cell. We show that the frequency and temporal correlation of impulses across afferent fibers determines which of four regimes of discharge activity is evoked. In the uncorrelated, here Poissonian, case, (i) cell discharge is determined by the total stimulation rate and temporal patterns of discharge are the same for different combinations of afferent fiber number and mean impulse rate per fiber giving the same total stimulation. Alternatively, if temporal correlations are present in the stimulus, (ii) for stimulation frequencies of 4 to at least 64 Hz there is a narrow range of afferent fiber number for which every stimulus pulse (composed of a single impulse on each afferent fiber) evokes a single action potential. In this case cell discharge is frequency locked to the stimulus with a concomitant reduction in discharge variability. (iii) For lower fiber numbers and thus discharge frequencies lower than the locking frequency, the variability of cell discharge is typically independent of afferent impulse timing, whereas, (iv) at higher fiber numbers and thus higher discharge frequencies, the reverse is true. We conclude that in case (iii) the cell acts as an integrator and discharge is determined by the stimulation rate, whereas in case (iv) the cell acts as a coincidence detector and the timing of discharge is determined by the temporal pattern of afferent stimulation. We discuss our results in terms of their significance for neuronal activity at the network level and suggest that the reported effects of varying stimulus timing and afferent convergence can be expected to obtain also with other principal cell types within the central nervous system.