A neural mechanism of phase-locked responses to sinusoidally amplitude-modulated signals in the inferior colliculus

Abstract

The central nucleus of the inferior colliculus (ICc) is an auditory region that receives convergent inputs from a large number of lower auditory nuclei. ICc neurons phase-lock to low frequencies of sinusoidally amplitude-modulated (SAM) signals but have a different mechanism in the phase-locking from that in neurons of lower nuclei. In the mustached bat, the phase-locking ability in lower nuclei is created by the coincidence of phase-locked excitatory and inhibitory inputs that have slightly different latencies. In contrast, the phase-locking property of ICc neurons is little influenced by the blocking of inhibitory synapses. Moreover, ICc neurons exhibit different characteristics in the spike patterns and synchronicity, classified here by three types of ICc neurons, or sustained, onset, and non-onset phase-locking neurons. However it remains unclear how ICc neurons create the phase-locking ability and the different characteristics. To address this issue, we developed a model of ICc neuronal population. Using this model, we show that the phase-locking ability of ICc neurons to low SAM frequencies is created by an intrinsic membrane property of ICc neuron, limited by inhibitory ion channels. We also show that response characteristics of the three types of neurons arise from the difference in an inhibitory effect sensitive to SAM frequencies. Our model reproduces well the experimental results observed in the mustached bat. These findings provide necessary conditions of how ICc neurons can give rise to the phase-locking ability and characteristic responses to low SAM frequencies.