Recovery cycle times of inferior colliculus neurons in the awake bat measured with spike counts and latencies

Riziq Sayegh,Siavosh Fazel-Pour,Paul A Faure,Brandon Aubie

doi:10.3389/fncir.2012.00056

Abstract

Neural responses in the mammalian auditory midbrain (inferior colliculus; IC) arise from complex interactions of synaptic excitation, inhibition, and intrinsic properties of the cell. Temporally selective duration-tuned neurons (DTNs) in the IC are hypothesized to arise through the convergence of excitatory and inhibitory synaptic inputs offset in time. Synaptic inhibition can be inferred from extracellular recordings by presenting pairs of pulses (paired tone stimulation) and comparing the evoked responses of the cell to each pulse. We obtained single unit recordings from the IC of the awake big brown bat (Eptesicus fuscus) and used paired tone stimulation to measure the recovery cycle times of DTNs and non-temporally selective auditory neurons. By systematically varying the interpulse interval (IPI) of the paired tone stimulus, we determined the minimum IPI required for a neuron's spike count or its spike latency (first- or last-spike latency) in response to the second tone to recover to within ≥50% of the cell's baseline count or to within 1 SD of it's baseline latency in response to the first tone. Recovery times of shortpass DTNs were significantly shorter than those of bandpass DTNs, and recovery times of bandpass DTNs were longer than allpass neurons not selective for stimulus duration. Recovery times measured with spike counts were positively correlated with those measured with spike latencies. Recovery times were also correlated with first-spike latency (FSL). These findings, combined with previous studies on duration tuning in the IC, suggest that persistent inhibition is a defining characteristic of DTNs. Herein, we discuss measuring recovery times of neurons with spike counts and latencies. We also highlight how persistent inhibition could determine neural recovery times and serve as a potential mechanism underlying the precedence effect in humans. Finally, we explore implications of recovery times for DTNs in the context of bat hearing and echolocation.

Highlights

The ability to extract temporal information from an acoustic signal is important for processing human speech (Denes, 1955), discriminating species-specific communication calls (Pollack and Hoy, 1979), localizing sounds (Knudsen and Konishi, 1979; Carr and Konishi, 1990), and echolocation by bats (Simmons, 1971, 1979; Suga and O’Neill, 1979; O’Neill and Suga, 1982)
Longpass duration-tuned neurons (DTNs) differ from typical sensory neurons in that they do not show a decrease in first-spike latency (FSL) with increasing stimulus amplitude that is typical of neurons that integrate stimulus energy (Brand et al, 2000; Faure et al, 2003; Pérez-González et al, 2006)
We found no obvious bias for recovery times measured with spike counts and FSLs because similar numbers of points fell above and below the unity lines at both levels above threshold (Figures 8A,B); recovery times measured with spike counts and FSLs tended to be longer than those measured with last-spike latency (LSL), as evidenced by a greater number of points falling below the unity lines in the scatterplots (Figures 8C–E)

Summary

Introduction

The ability to extract temporal information from an acoustic signal is important for processing human speech (Denes, 1955), discriminating species-specific communication calls (Pollack and Hoy, 1979), localizing sounds (Knudsen and Konishi, 1979; Carr and Konishi, 1990), and echolocation by bats (Simmons, 1971, 1979; Suga and O’Neill, 1979; O’Neill and Suga, 1982). Neurons with spiking responses selective for signal duration, known as duration-tuned neurons (DTNs), provide one neural mechanism for encoding temporal information. The biological function(s) of DTNs to hearing is(are) unknown; the range of neural best durations (BD) within a species (BD = stimulus duration that causes maximum spiking) correlates with the range of vocalization durations of species-specific communication sounds in non-echolocating vertebrates and with biosonar pulse durations in echolocating bats (for reviews, see Sayegh et al, 2011; Jen et al, 2012)

Methods

Results

Discussion

Conclusion