Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing

Abstract

Short-term adaptation was examined in single unit recordings from 113 superior olive neurons of anaesthetized 3- to 6-month-old Long–Evans rats. Responses to an equal intensity BF probe tone presented 1 ms after an ‘adapting’ BF tone were adapted by 56.3±2.6% (mean±S.E.) compared to responses at a 512 ms delay. The rapid decrease in discharge rate during adapting tones often approximated exponential time courses with time constants of less than 20 ms. The recovery from adaptation was exponential with time constants of 106±20.0 ms. The magnitude of adaptation and time course of recovery following monaural stimulation of binaurally excited (EE) neurons were not significantly different in both input pathways. Additionally, in 60% of EE neurons, an ‘adapting’ tone presented to one ear reduced subsequent responses to probe tones presented to the opposite ear. Binaural stimulation resulted in equal or greater adaptation of responses than monaural stimulation of either ear. The recovery of binaural excitatory responses generally followed a time course between recovery functions for ipsilateral and contralateral monaural stimuli. Lateral Superior Olive (LSO) neurons encode sound source location through the interaction of ipsilateral excitation and contralateral inhibition (IE). Ipsilaterally driven excitatory responses in LSO neurons exhibited the greatest magnitude of adaptation (68.5±21.1%). Adaptation of inhibition was observed in over half of IE neurons. Responses of LSO neurons to binaural BF probe stimuli were greatest immediately after a 200 ms BF ‘inhibitory adapting’ stimulus to the contralateral ear, and decreased with greater interstimulus delays. Responses to binaural stimulation were constant after prior binaural adaptation, when the magnitude and recovery of adaptation to monaural stimuli were similar for excitation and inhibition (8/25 IE cells). The functional significance and possible sites of adaptation processes are discussed.