Physiological Basis of Noise-Induced Hearing Loss in a Tympanal Ear

Abstract

Acoustic overexposure, such as listening to loud music too often, results in noise-induced hearing loss. The pathologies of this prevalent sensory disorder begin within the ear at synapses of the primary auditory receptors, their postsynaptic partners and their supporting cells. The extent of noise-induced damage, however, is determined by over-stimulation of primary auditory receptors, upstream of where the pathologies manifest. A systematic characterisation of the electrophysiological function of the upstream primary auditory receptors is warranted to understand how noise-exposure impacts on downstream targets, where the pathologies of hearing loss begin. Here, we used the experimentally-accessible locust ear (male, Schistocerca gregaria) to characterise a decrease in the auditory receptor's ability to respond to sound after noise exposure. Surprisingly, after noise exposure, the electrophysiological properties auditory receptors remains unchanged, despite a decrease in the ability to transduce sound. This auditory deficit stems from changes in a specialised receptor lymph that bathes the auditory receptors-revealing striking parallels with the mammalian auditory system. Significance Statement Noise exposure is the largest preventable cause of hearing loss. It is the auditory receptors that bear the initial brunt of excessive acoustic stimulation, because they must convert excessive soundinduced movements into electrical signals, but remain functional afterward. Here we use the accessible ear of an invertebrate to-for the first time in any animal-characterise changes in auditory receptors after noise overexposure. We find that their decreased ability to transduce sound into electrical signals is, most probably, due to changes in supporting (scolopale) cells that maintain the ionic composition of the ear. An emerging doctrine in hearing research is that vertebrate primary auditory receptors are surprisingly robust, something which we show rings true for invertebrate ears too.

Gene transcription changes in a locust model of noise-induced deafness

“…Details of the animal handling, noise exposure, and transcriptome creation have been given before ( 3 ). Briefly, locusts ( Schistocerca gregaria ) were reared in the gregarious phase with a 12-h light/dark cycle at 36.25°C, fed on a combination of fresh wheat and bran ad libitum.…”

“…The searches were conducted at relatively low stringency so that many unrelated genes were also found, assembled, and included in the list. Transcripts from this targeted approach included the genes that we described previously ( 3 ).…”

“…Desert locusts, Schistocerca gregaria, have paired abdominal auditory organs, each consisting of an external tympanum with a sensory structure called M € uller's organ attached internally (21)(22)(23). We found previously that 24-h noise exposure produced hearing loss characterized by both mechanical and electrophysiological changes in the locust system (3). Here, we compared the abundances of 500 different mRNA transcripts from M€ uller's organs in noise-exposed versus control locusts, in attempts to identify the major molecular changes underway in this model of noise-induced hearing loss.…”

“…About 1.5 billion people globally have compromised hearing (World Health Organization, http://www.who.int/ ) due to a range of causes, including genetic defects, infectious diseases, loud noise exposure, and aging. Experimental noise exposure has provided important models of deafness in mammals ( 1 ), and this has recently been extended to insect auditory systems ( 2 , 3 ). Despite obvious differences, insects have evolved organs of hearing that deal with the same problems in converting the small pressure differences of sound into receptor currents in sensory neurons ( 4 ).…”

“…Deafness could involve malfunction at any of the three stages. Changes in mechanical properties and reductions in transduced receptor potentials have been seen in aged ( 7 ) and noise-exposed ( 2 , 3 ) insects, but the causes of these changes remain enigmatic.…”