University of Sussex June 7, 2017 Brighton

In this article, we investigate whether mice can respond to low-frequency sounds. We demonstrate that low-frequency pure tones, which have stimulus parameters outside the sensitivity range of the mouse cochlea, can facilitate acoustic startle responses caused by a high-frequency tone that is within the range of the frequency and sensitivity of the cochlea. This facilitation disappears in vestibular deficient mice proving that the vestibular system in mice can mediate the detection of low-frequency sounds.”

By Gareth P. Jones, Victoria A. Lukashkina, Ian J. Russell and Andrei N. Lukashkin
School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK

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.

Introduction

Mammals have a remarkable sense of hearing, with auditory ranges specifically adapted to their particular acoustic niche. This sensitivity is achieved mainly by the cochlea, a relatively new evolutionary adaptation compared with the much more ancient vestibular system. Recent studies have demonstrated, however, that parts of the mammalian vestibular system, notably the sacculus, historically one of the first acoustically sensitive organs (Popper et al. 1982), have retained the ability to detect acoustic stimuli previously associated only with the cochlea. There is further evidence that this stimulation may have behavioral significance (Todd 2001). Acoustic sensitivity of the sacculus in mammals might be expected as consequences of both its evolutionary history and anatomical location. In mice, for example, the sacculus is located behind the oval window membrane, directly in the line of vibration caused by movement of the stapes. It is clearly visible through the oval window once the stapes have been removed.

The vestibular systems of birds and mammals including cats (McCue and Guinan 1994, 1995), monkeys (Young et al. 1977), guinea pigs (Cazals et al. 1983; Didier and Cazals 1989), and pigeons (Wit et al. 1984) have been found to respond to acoustic stimuli, often with good evidence that the vestibular afferents innervating the sacculus are the most acoustically sensitive. Evidence from primates indicates that afferent projections from the sacculus reach the medial vestibular nucleus or inferior vestibular nucleus, which then projects bilaterally to the spinal cord (Stein and Carpenter 1967). In humans, for example, this pathway mediates vestibular-evoked myogenic potentials (VEMPs), in which acoustic excitation of the vestibular system causes twitches in various muscles, most obviously the cervical muscles (Bickford et al. 1964; Ferber-Viart et al. 1999). Although the typical stimuli used are also within the human auditory range, an auditory origin of the VEMPS is ruled out by the fact that they still occur in patients with hearing loss (Sheykholeslami and Kaga 2002; Wang and Young 2003; Murofushi et al. 2005).

With its ability to respond to acoustical stimulation, the vestibular system has the potential to extend the hearing range of mammals and hence their ability to detect low frequency sounds of behavioral significance. For example, the frequency range of the mouse cochlea, defined by sensitivity to sound stimulation below 80 dB SPL, is approximately 4–75 kHz, although this varies depending on age and mouse strain (Nyby 2001). There are three areas of peak sensitivity that coincide with behaviorally relevant frequency ranges; the area of best sensitivity at the lower range is around 10–18 kHz and at ultrasonic frequencies, 40 kHz and 70±10 kHz (Nyby 2001; Müller et al. 2005).

In this article, we investigate whether mice can respond to low-frequency sounds. We demonstrate that low-frequency pure tones, which have stimulus parameters outside the sensitivity range of the mouse cochlea (Taberner and Liberman 2005; Müller et al. 2005), can facilitate acoustic startle responses (ASRs) caused by a high-frequency tone that is within the range of the frequency and sensitivity of the cochlea (Fig. 1). This facilitation disappears in vestibular deficient mice proving that the vestibular system in mice can mediate the detection of low-frequency sounds.