Abstract

Acoustic stimuli are often represented in the early auditory pathway as patterns of neural activity synchronized to time-varying features. This phase-locking predominates until the level of the medial geniculate body (MGB), where previous studies have identified two main, largely segregated response types: Stimulus-synchronized responses faithfully preserve the temporal coding from its afferent inputs, and Non-synchronized responses, which are not phase locked to the inputs, represent changes in temporal modulation by a rate code. The cellular mechanisms underlying this transformation from phase-locked to rate code are not well understood. We use a computational model of a MGB thalamocortical neuron to test the hypothesis that these response classes arise from inferior colliculus (IC) excitatory afferents with divergent properties similar to those observed in brain slice studies. Large-conductance inputs exhibiting synaptic depression preserved input synchrony as short as 12.5 ms interclick intervals, while maintaining low firing rates and low-pass filtering responses. By contrast, small-conductance inputs with Mixed plasticity (depression of AMPA-receptor component and facilitation of NMDA-receptor component) desynchronized afferent inputs, generated a click-rate dependent increase in firing rate, and high-pass filtered the inputs. Synaptic inputs with facilitation often permitted band-pass synchrony along with band-pass rate tuning. These responses could be tuned by changes in membrane potential, strength of the NMDA component, and characteristics of synaptic plasticity. These results demonstrate how the same synchronized input spike trains from the inferior colliculus can be transformed into different representations of temporal modulation by divergent synaptic properties.

Highlights

  • The auditory system rapidly analyzes and processes temporal modulations encoded in acoustic stimuli such as speech and animal vocalizations [1]

  • In the inferior colliculus (IC), which serves as the primary auditory input to the auditory thalamus, neurons fire action potentials that generally exhibit correlated rate and synchronization tuning to modulation frequency, with most neurons synchronized at some modulation frequency [1,2,3]

  • For the None condition, AMPA and NMDA conductances were used without short-term plasticity, meaning no paired pulse depression or facilitation (Fig. 1E, red traces)

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Summary

Introduction

The auditory system rapidly analyzes and processes temporal modulations encoded in acoustic stimuli such as speech and animal vocalizations [1]. In the inferior colliculus (IC), which serves as the primary auditory input to the auditory thalamus, neurons fire action potentials that generally exhibit correlated rate and synchronization tuning to modulation frequency, with most neurons synchronized at some modulation frequency [1,2,3]. This is not the case in auditory thalamus and cortex. From this data there is evidence of a transformation from temporal encoding in the IC to rate encoding in the MGB over a restricted frequency range

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