A mathematical analysis of spatiotemporal summation of auditory nerve firings

Abstract Many theories of hearing hypothesize that spatiotemporal combination of single-fiber activity forms an important feature of the auditory system. One mechanism which has been proposed to explain perceptual performance is spatiotemporal summation of Auditory Nerve (AN) firings. Anatomical and physiological studies have found a number of different cell types in the Cochlear Nucleus (CN) which appear to perform such summations. The purpose of this paper is to determine theoretically how various degrees of AN fiber convergence onto summing neurons in the CN would affect estimation and discrimination of stimulus features from the summing neurons' outputs. To achieve this, we utilize an analytical model, based on a point process representation of AN activity, which includes parameterized measures of stimulus properties. The summing neuron model allows for an arbitrary degree of AN fiber convergence, thus facilitating an investigation of the feasibility of theories of neural coding of sound for different summing neuron types. Results obtained from the model indicate that for coding of the stimulus frequency in the periodicity of firings, the optimal spread of input fibers is very narrow and temporal integration is very short. This suggests that AN fibers which converge onto CN cells exhibiting enhanced synchronization originate from sites on the basilar membrane very close together. In contrast, CN cell types which exhibit reduced synchronization could be useful in performing estimation and discrimination tasks based on the average discharge rate. The model indicates that this could be achieved by a very wide spread of inputs and/or long-term temporal integration. We postulate that a wide spread of inputs would be preferential to long-term temporal integration, because this would enable the neuron's output to follow rapid changes in the average discharge rate of a population of fibers. Consequently, transients in the stimulus intensity which produce rapid changes in the average discharge rate of a population of fibers could be detected by a rapid change in the output of such a summing neuron.