Influence of envelope waveform on ITD sensitivity of neurons in the auditory midbrain

• Published in: Journal of neurophysiology Vol. 118; no. 4; pp. 2358 - 2370
• Main Authors: Greenberg, David, Monaghan, Jessica J M, Dietz, Mathias, Marquardt, Torsten, McAlpine, David
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01-10-2017
• Series: Sensory Processing
• Subjects: Animals; Auditory Perception; Evoked Potentials, Auditory; Guinea Pigs; Mesencephalon - cytology; Mesencephalon - physiology; Neurons - physiology; Reaction Time; ITD-sensitive neurons; envelope ITD; amplitude modulated
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.01048.2015

Interaural time differences (ITDs) conveyed by the modulated envelopes of high-frequency sounds can serve as a cue for localizing a sound source. Klein-Hennig et al. (
129: 3856, 2011) demonstrated the envelope attack (the rate at which stimulus energy in the envelope increases) and the duration of the pause (the interval between successive envelope pulses) as important factors affecting sensitivity to envelope ITDs in human listeners. Modulated sounds with rapid attacks and long pauses produce the lowest ITD discrimination thresholds. The duration of the envelope's sustained component (sustain) and the rate at which stimulus energy falls at the offset of the envelope (decay) are only minor factors. We assessed the responses of 71 single neurons, recorded from the midbrains of 15 urethane-anesthetized tri-colored guinea pigs, to envelope shapes in which the four envelope components, i.e., attack, sustain, decay, and pause, were systematically varied. We confirmed the importance of the attack and pause components in generating ITD-sensitive responses. Analysis of neural firing rates demonstrated more neurons (49/71) show ITD sensitivity in response to "damped" stimuli (fast attack and slow decay) compared with "ramped" stimuli (slow attack and fast decay) (14/71). Furthermore, the lowest threshold for the damped stimulus (91 μs) was lower by a factor of 4 than that for the temporally reversed ramped envelope shape (407 μs). The data confirm the importance of fast attacks and optimal pause durations in generating sensitivity to ITDs conveyed in the modulated envelopes of high-frequency sounds and are incompatible with models of ITD processing based on the integration of sound energy over time.
Using single-neuron electrophysiology, we show that the precise shape of a sound's "energy envelope" is a critical factor in determining how well midbrain neurons are able to convey information about auditory spatial cues. Consistent with human behavioral performance, sounds with rapidly rising energy and relatively long intervals between energy bursts are best at conveying spatial information. The data suggest specific sound energy patterns that might best be applied to hearing devices to aid spatial listening.