Timing of sound-evoked potentials and spike responses in the inferior colliculus of awake bats

Abstract

Neurons in the inferior colliculus (IC), one of the major integrative centers of the auditory system, process acoustic information converging from almost all nuclei of the auditory brain stem. During this integration, excitatory and inhibitory inputs arrive to auditory neurons at different time delays. Result of this integration determines timing of IC neuron firing. In the mammalian IC, the range of the first spike latencies is very large (5-50 ms). At present, a contribution of excitatory and inhibitory inputs in controlling neurons' firing in the IC is still under debate. In the present study we assess the role of excitation and inhibition in determining first spike response latency in the IC. Postsynaptic responses were recorded to pure tones presented at neuron's characteristic frequency or to downward frequency modulated sweeps in awake bats. There are three main results emerging from the present study: (1) the most common response pattern in the IC is hyperpolarization followed by depolarization followed by hyperpolarization, (2) latencies of depolarizing or hyperpolarizing responses to tonal stimuli are short (3-7 ms) whereas the first spike latencies may vary to a great extent (4-26 ms) from one neuron to another, and (3) high threshold hyperpolarization preceded long latency spikes in IC neurons exhibiting paradoxical latency shift. Our data also show that the onset hyperpolarizing potentials in the IC have very small jitter (<100 micros) across repeated stimulus presentations. The results of this study suggest that inhibition, arriving earlier than excitation, may play a role as a mechanism for delaying the first spike latency in IC neurons.

Suppression of spontaneous firing in inferior colliculus neurons during sound processing

“…It has also been demonstrated that neurons exhibiting forward suppression that persists for hundreds of milliseconds do not show inhibitory conductances for longer than 50–100 ms. In our present and previous intracellular studies (Voytenko and Galazyuk 2007, 2008), we also rarely observed membrane hyperpolarizations in the IC lasting longer than 50 ms, even though suppression can last for hundreds of milliseconds. In an attempt to identify a possible cellular mechanism underlying this long-lasting suppression, we tested whether input resistance in IC neurons was altered during the suppression.…”

“…9A, C, E). When the sound level was increased to 80 dB SPL, this neuron showed typical response patterns for IC neurons: IPSP-EPSP-spike-IPSP (Voytenko and Galazyuk, 2007, 2008; Peterson et al, 2008) followed by a suppression of spontaneous firing that lasted about 100 ms (Fig. 9B).…”

“…In vivo intracellular recordings in the IC have revealed hyperpolarizations that exceed the duration of the sound stimulus in many neurons (Nelson and Erulkar 1963; Torterolo et al 1995; Covey et al 1996; Kuwada et al 1997; Pedemonte et al 1997, Voytenko and Galazyuk 2007; 2008; Peterson et al, 2008). However, these potentials lasted less than 100 ms after the end of a stimulus, even in barbiturate anesthetized animals (Covey et al 1996; Kuwada et al 1997; Pedemonte et al 1997).…”

Exponential modeling of human frequency-following responses to voice pitch

“…30 dB nHL). This fi nding can be explained, at least partially, by the fact that high stimulus intensities produce better neural-fi ring effi ciency and less temporal jitter in single neuron recordings in the auditory nerve (Miller et al, 2006;Imennov & Rubinstein, 2009), and brainstem nuclei (Keller & Takahashi, 2000;Voytenko & Galazyuk, 2008). Briefl y, fi ring effi ciency can be computed as a ratio of the number of neuronal spikes elicited and the number of times the stimulus is presented.…”

First-Spike Latency in the Presence of Spontaneous Activity

“…It has been shown previously that the first-spike latency contains important information in auditory, visual, olfactory, and somatosensory modalities (Furukawa & Middlebrooks, 2002;Kalluri & Delgutte, 2003;Panzeri, Petersen, Schultz, Lebedev, & Diamond, 2001;Reich, Mechler, & Victor, 2001;Rospars, Lansky, Duchamp, & DuchapViret, 2003). Namely, experimental results have demonstrated that spike timing carries additional information to the spike rate (Wiener & Richmond, 2003;Voytenko & Galazyuk, 2008;Perrinet, Samuelides, & Thorpe, 2004;. Due to these reasons, determination of the response latencies of one or more neurons was studied under different situations.…”