On the precision of neural computation with interaural level differences in the lateral superior olive

Interaural level difference (ILD) is one of the basic binaural clues in the spatial localization of a sound source. Due to the acoustic shadow cast by the head, a sound source out of the medial plane results in an increased sound level at the nearer ear and a decreased level at the distant ear. In the mammalian auditory brainstem, the ILD is processed by a neuronal circuit of binaural neurons in the lateral superior olive (LSO). These neurons receive major excitatory projections from the ipsilateral side and major inhibitory projections from the contralateral side. As the sound level is encoded predominantly by the neuronal discharge rate, the principal function of LSO neurons is to estimate and encode the difference between the discharge rates of the excitatory and inhibitory inputs. Two general mechanisms of this operation are biologically plausible: (1) subtraction of firing rates integrated over longer time intervals, and (2) detection of coincidence of individual spikes within shorter time intervals. However, the exact mechanism of ILD evaluation is not known. Furthermore, given the stochastic nature of neuronal activity, it is not clear how the circuit achieves the remarkable precision of ILD assessment observed experimentally. We employ a probabilistic model and complementary computer simulations to investigate whether the two general mechanisms are capable of the desired performance. Introducing the concept of an ideal observer, we determine the theoretical ILD accuracy expressed by means of the just-noticeable difference (JND) in dependence on the statistics of the interacting spike trains, the overall firing rate, detection time, the number of converging fibers, and on the neural mechanism itself. We demonstrate that the JNDs rely on the precision of spike timing; however, with an appropriate parameter setting, the lowest theoretical values are similar or better than the experimental values. Furthermore, a mechanism based on excitatory and inhibitory coincidence detection may give better results than the subtraction of firing rates. This article is part of a Special Issue entitled Neural Coding 2012.