Abstract
Author SummaryAnimals can locate the source of a sound by detecting microsecond differences in the arrival time of sound at the two ears. Neurons encoding these interaural time differences (ITDs) receive an excitatory synaptic input from each ear. They can perform a microsecond computation with excitatory synapses that have millisecond time scale because they are extremely sensitive to the input's “rise time,” the time taken to reach the peak of the synaptic input. Current theories assume that the biophysical properties of the two inputs are identical. We challenge this assumption by showing that the rise times of excitatory synaptic potentials driven by the ipsilateral ear are faster than those driven by the contralateral ear. Further, we present a computational model demonstrating that this disparity in rise times, together with the neurons' sensitivity to excitation's rise time, can endow ITD-encoding with microsecond resolution in the biologically relevant range. Our analysis also resolves a timing mismatch. The difference between contralateral and ipsilateral latencies is substantially larger than the relevant ITD range. We show how the rise time disparity compensates for this mismatch. Generalizing, we suggest that phasic-firing neurons—those that respond to rapidly, but not to slowly, changing stimuli—are selective to the temporal ordering of brief inputs. In a coincidence-detection computation the neuron will respond more robustly when a faster input leads a slower one, even if the inputs are brief and have similar amplitudes.
Highlights
In order to localize acoustic objects along the horizontal plane, the nervous system is able to distinguish microsecond differences in the arrival time of sound at the two ears, referred to as interaural time differences (ITDs)
We confirmed that synaptic inhibition reduced the effect of shifting the ITD response function towards zero ITD, and leads us to suggest that the compensation arises from the excitatory asymmetry described above (Figure 1). How can such a small asymmetry in excitatory post-synaptic potential (EPSP) slope influence ITD sensitivity in medial superior olivary neurons (MSO) neurons? We addressed this question by using a computational MSO neuron model that was driven by bilateral trains of excitatory and inhibitory inputs temporally modulated with a periodic function representing ventral cochlear nucleus (VCN) responses to pure tone stimuli
Using only differences in vector strength of the simulated inputs from the VCN arriving to each dendrite of the MSO neuron model we modeled differences in rising slope of the bilateral EPSPs (Notice: without delaying the composite EPSP peak, see triangles in Figure 3 for excitatory postsynaptic conductances (EPSGs) peaks)
Summary
In order to localize acoustic objects along the horizontal plane, the nervous system is able to distinguish microsecond differences in the arrival time of sound at the two ears, referred to as interaural time differences (ITDs). Low sound frequencies are the most useful signals for detecting ITDs, and animals with good sensitivity below 1,500 Hz tend to perform best at this perception [1]. In mammals this computation is first performed by medial superior olivary neurons (MSO) in the auditory brain stem. Each MSO neuron receives two sets of excitatory inputs on its bipolar dendrites, with each set activated by one ear. When both excitatory pathways are activated within a narrow time window, the MSO neuron detects the coincident excitatory synaptic inputs and fires action potentials. An ITD response function is the representation of the variation of MSO discharge rate with the relative delay of the two inputs and, the position of a sound along the horizontal plane [2]
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