Abstract
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. (J Acoust Soc Am 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.NEW & NOTEWORTHY 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.
Highlights
NEW & NOTEWORTHY 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
Raster plots (Fig. 2, C and D, left) show responses to characteristic frequency (CF) tones modulated with sinusoidally amplitude-modulated (SAM) or pseudo square-wave (PSW) modulation shapes, and interaurally delayed over a range of interaural time differences (ITDs) between Ϫ8.33 and 15 ms in steps of 1.67 ms
ITD tuning is present for the PSW envelope shape, indicated by higher discharge rates at favorable ITDs and reduced rates at unfavorable ITDs, compared with the SAM envelope shape, for which discharge rates remain low across all envelope ITDs assessed
Summary
NEW & NOTEWORTHY 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. The classic duplex theory of binaural hearing (Strutt 1907) posits that humans exploit interaural time differences (ITDs) predominantly for localizing low-frequency (Ͻ1,500 Hz) sound sources by virtue of sensitivity to the ongoing temporal fine structure at each ear. Listeners are able to exploit ITDs conveyed in the modulated envelopes of high-frequency sounds to perform spatial listening tasks (Bernstein and Trahiotis 1994, 2002; Henning 1974; Klumpp and Eady 1956; McFadden and Pasanen 1976; Nuetzel and Hafter 1976) In cases of both lowand high-frequency sounds, physiological sensitivity to ITDs relies on the generation of action potentials at the synapse of the inner hair cells, phase-locked to either the stimulus fine structure for low-frequency sounds or to the stimulus envelope for high-frequency sounds. Many existing models of binaural interaction cannot explain this difference, because their performance often depends on the spectrum of the preprocessed signal (Bernstein and Trahiotis 1996; Dietz et al 2012), which is identical in the case of the time-reversed ramped and damped stimuli (see Fig. 1C)
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