The vestibular system mediates sensation of low-frequency sounds in mice

Abstract

The mammalian inner ear contains sense organs responsible for detecting sound, gravity and linear acceleration, and angular acceleration. Of these organs, the cochlea is involved in hearing, while the sacculus and utriculus serve to detect linear acceleration. Recent evidence from birds and mammals, including humans, has shown that the sacculus, a hearing organ in many lower vertebrates, has retained some of its ancestral acoustic sensitivity. Here we provide not only more evidence for the retained acoustic sensitivity of the sacculus, but we also found that acoustic stimulation of the sacculus has behavioral significance in mammals. We show that the amplitude of an elicited auditory startle response is greater when the startle stimuli are presented simultaneously with a low-frequency masker, including masker tones that are outside the sensitivity range of the cochlea. Masker-enhanced auditory startle responses were also observed in otoconia-absent Nox3 mice, which lack otoconia but have no obvious cochlea pathology. However, masker enhancement was not observed in otoconia-absent Nox3 mice if the low-frequency masker tones were outside the sensitivity range of the cochlea. This last observation confirms that otoconial organs, most likely the sacculus, contribute to behavioral responses to low-frequency sounds in mice.

FIG. 1

ASR (circles; age 1 month) and ABR (squares) thresholds for CBA mice compared with the levels and frequencies used as background maskers in the experiments (triangles). Only the higher levels (60 and 80 dB SPL) at the higher frequencies (3 and 6 kHz) are above ABR threshold. ASR threshold curve was modified from Parham and Willott (1988). ABR threshold curve was modified from Müller et al. (2005).

FIG. 2

A The startle chamber schematic. B The temporal order of probe alone presentations. C The temporal order of probe and masker presentations (C). The onset of the masker preceded that of the probe by 2,000 ms and continued for a total of 3,000 ms.

FIG. 3

Startle ratio (startle amplitude, compared with that due to the probe tone on its own; y = 1) as a function of masker frequency for CBA mice. A 80-dB SPL, 14-kHz probe. B 90-dB SPL, 14-kHz probe. In this and all subsequent figures, startle ratio is the ASR due to the combination of probe tone and masker (P_M) divided by the ASR to the probe tone alone (P₀) (P_M/P₀). Error bars indicate standard deviation; * indicates significance at p ≤ 0.0, n = 7, for 40- and 60-dB SPL points for both probes and n = 8 for all 80-dB SPL maskers.

FIG. 4

Threshold levels of acoustical responses (A) recorded in nine otoconia-present (black) and three otoconia-absent (gray) mice and neural responses (B) recorded in five otoconia-present (black) and three otoconia-absent (gray) mice. A Threshold level L1 (mean ± SD) of the low-frequency primary f1 required to generate 0-dB SPL DPOAE at frequency 2f1–f2 for different frequencies of the high-frequency primary f2. B CAP threshold levels (mean ± SD) for pure-tone stimulation. Number of animals n is indicated within the figure panels.

FIG. 5

Startle ratio (startle amplitude, compared with that due to the probe tone on its own; y = 1) as a function of masker frequency for otoconia-present Nox3 mice at the masker levels shown. n = 4 for all points.

FIG. 6

Startle ratio (startle amplitude, compared with that due to the probe tone on its own; y = 1), as a function of masker frequency for otoconia-absent Nox3 mice at the masker levels shown. n = 4 for all points.

FIG. 7

Startle ratio (startle amplitude, compared with that due to the probe tone on its own; y = 1), as a function of masker frequency at constant 80-dB SPL level for CBA, otoconia-present (OP) Nox3, and otoconia absent (OA) Nox3 mice.