Elsevier

Hearing Research

Volume 171, Issues 1–2, September 2002, Pages 82-95
Hearing Research

Behavioral and evoked-potential thresholds in young and old Mongolian gerbils (Meriones unguiculatus)

https://doi.org/10.1016/S0378-5955(02)00454-9Get rights and content

Abstract

Age-dependent hearing loss has been well documented in gerbils exceeding 2 years of age using physiological methods (e.g. [Mills et al. (1990) Hear. Res. 46, 201–210]). We determined behavioral thresholds for broad-band noise and pure-tone pulses in gerbils as a function of age. Contrary to expectations based on previously published physiological data, we found no significant (broad-band noise and 10 kHz) or only a very small hearing loss (7 dB at 2 kHz) in 30–36-month-old animals. In animals over 3 years of age we observed an increased spread of thresholds and threshold shifts exceeding 20 dB in some individuals. Behavioral thresholds of old gerbils from two breeding colonies (University of Regensburg and Medical University of South Carolina) were similar. Data from individual animals where thresholds were determined physiologically and behaviorally indicate that results from auditory brainstem response measurements show no shift at 18 months while subsequent measurements at 28–29 months revealed age-dependent threshold shifts of 10–15 dB. In contrast, thresholds determined by behavioral methods in these same individuals at 31–33 months of age remained stable.

Introduction

Hearing loss is an increasing problem in the industrialized countries because the increasing life span leads to a growing proportion of aged individuals. Large studies in Great Britain and Australia have shown that hearing impairment affects 15–20% of the adult population (Davis, 1989, Davis, 1990, Wilson et al., 1999). However, hearing impairment is not distributed uniformly across age, since it affects predominantly the elderly; 80% of the hearing-impaired adults are over 60 years of age (Davis, 1990). In humans, hearing loss begins between 30 and 40 years of age and progresses in a frequency-specific fashion with increasing age, affecting low frequencies less than high frequencies (review: Davis, 1997). Depending on the age group and the definition of hearing loss, 40–80% of aged subjects are affected (Kim et al., 2000, Cruickshanks et al., 1998, Moscicki et al., 1985) illustrating the magnitude of the problem. Several different types of age-dependent hearing loss in humans have been associated with specific forms of cochlear pathology (Schuknecht and Gacek, 1993). Thus animal models need to be developed and characterized to investigate age-dependent hearing loss under controlled experimental conditions in more detail.

A number of studies have been performed in rodents including guinea pigs (Nozawa et al., 1996, Ingham et al., 1998, Proctor et al., 1998), chinchillas (McFadden et al., 1997), different strains of rats (Cooper et al., 1990, Turnock and Harrison, 1975, Borg, 1982) and mice (Zheng et al., 1999, Willott, 1986, Ehret, 1974), typically demonstrating hearing loss in aged animals that was more pronounced at high frequencies. In addition to the species mentioned above, the Mongolian gerbil (Meriones unguiculatus) is becoming an increasingly popular model in auditory research. In contrast to mice and rats, the behavioral threshold curve of the gerbil shows high sensitivity from 1 to 10 kHz, which is quite similar to that of humans (Ryan, 1976). In contrast to chinchilla and guinea pig, gerbils have a shorter life span of 3–4 years (Cheal, 1986, Mills et al., 1990).

A number of physiological studies using auditory brainstem responses (ABRs), compound action potential (CAP) measurements and recordings of single auditory nerve fibers provide evidence for and characterize age-dependent hearing loss in the gerbil. Threshold elevation becomes evident at an age of 2 years (10–15 dB loss). At 3 years of age the hearing loss is 15–20 dB at 1–2 kHz and 25–30 dB at 8–16 kHz (Mills et al., 1990, Hellstrom and Schmiedt, 1990, Hellstrom and Schmiedt, 1996, Tarnowski et al., 1991). Anatomical data suggest that hair-cell loss is not directly correlated with the observed high-frequency hearing loss (Tarnowski et al., 1991). However, changes in the stria vascularis and loss of the endocochlear potential (EP) seem to be responsible for or contribute to the observed threshold elevations (Schulte and Schmiedt, 1992, Gratton et al., 1995, Mills et al., 1996). We are aware of only one behavioral study investigating age-dependent threshold shifts and comparing domesticated laboratory gerbils and wild-type gerbils (Sinnot et al., 1997). In the domesticated gerbils the thresholds for the detection of vowels increased 10 dB per year between 12 and 36 months of age, resembling results of age-dependent hearing loss from physiological studies at low frequencies (Sinnot et al., 1997). In contrast to these results, Sinnot et al. (1997) did not find a comparable threshold increase in wild-type gerbils. Since the responses to the vowels were predominantly to F1 frequencies below 1 kHz (Sinnot et al., 1997), we wanted to determine behavioral thresholds for pure tones to compare behavioral thresholds and age-dependent hearing loss with physiologically determined data in the gerbil.

The collection of behavioral data in the gerbil was motivated by recent data in aged human subjects, which suggested a discrepancy in the observed age-dependent hearing loss of up to 20 dB between behavioral pure-tone thresholds and physiologically determined ABR thresholds (Mills et al., 2001, submitted for publication). To further strengthen this comparison of methods for threshold determination in the gerbil and to investigate potential differences between different gerbil breeding lines, we analyzed animals from two colonies. One group of animals was from our Regensburg (RB) strain where significant morphological differences in cochlear nucleus morphology compared to wild-type gerbils have recently been documented (Gleich et al., 2000). The second group included gerbils from the breeding colony of the Medical University of South Carolina (SC, USA) because most of the published physiological data have been obtained from this strain. In addition, we were able to directly compare physiologically and behaviorally determined thresholds that have been measured in five individuals using the two methods.

Section snippets

Subjects

Subjects were 26 Mongolian gerbils (M. unguiculatus) of the RB strain (RB gerbils) which were bred in the animal facilities of the University of Regensburg (Gleich et al., 2000). In a group of young animals (three male and seven female) testing began at an age of 3 months and most data were collected before they reached an age of 12 months. An additional gerbil that could not be trained within 3 weeks was not tested further. In two animals of this group data collection was extended to the age

Behavioral training

The training of the 26 RB gerbils, beginning with the first training session in the experimental setup to the first valid threshold estimate for broad-band noise, took on average 2 weeks with a maximum of about 4 weeks in one gerbil. After learning the threshold-detection task for broad-band noise, it was generally easy for the animals to switch from broad-band noise to pure-tone stimuli. Most of the RB gerbils gave valid thresholds for the new task within 9 days. There was only one young

Psychoacoustic thresholds in gerbils

The comparison between thresholds of young RB gerbils and 30–36-month-old RB and SC gerbils revealed a significant difference between the young and each group of old gerbils only for the 2 kHz test signal. This difference, however, was only 5–9 dB and would not be considered as a hearing loss by audiologists. There was no significant difference between these age groups with respect to the 10 kHz and the broad-band noise test signals, despite the expected threshold difference based on previous

Conclusions

The data presented here show that behavioral thresholds in gerbils remain stable up to 3 years of age while ABR thresholds are elevated in 2-year-old gerbils. Threshold loss determined by both methods (ABR and behavior) differs in old animals. This observation is relevant for interpreting the diagnostic evaluation of hearing loss in older subjects as determined by ABR or pure-tone audiometry.

Acknowledgements

We thank S. Kopetschek and C. Weyers for help with animal care and behavioral testing. Supported by the DFG (Str. 275/4-1) and NIH/NIA RO1 AG15705 (F.A.B.) and RO1 AG14748 (R.A.S.).

References (61)

  • L.I. Hellstrom et al.

    Rate/level functions of auditory nerve fibers in young and quiet-aged gerbils

    Hear. Res.

    (1991)
  • S.L. McFadden et al.

    Age-related decline of auditory function in the chinchilla (Chinchilla laniger)

    Hear. Res.

    (1997)
  • M.D. McGinn et al.

    Auditory experience affects degeneration of the ventral cochlear nucleus in Mongolian gerbils

    Hear. Res.

    (1987)
  • J.H. Mills et al.

    Age-related changes in auditory potentials of Mongolian gerbils

    Hear. Res.

    (1990)
  • E.M. Ngan et al.

    Relationship between the auditory brainstem response and auditory nerve thresholds in cats with hearing loss

    Hear. Res.

    (2001)
  • E.M. Ostapoff et al.

    A degenerative disorder of the central auditory system of the gerbil

    Hear. Res.

    (1989)
  • R.A. Schmiedt

    Effects of aging on potassium homeostasis and the endocochlear potential in the gerbil cochlea

    Hear. Res.

    (1996)
  • R.A. Schmiedt et al.

    Tuning and suppression in auditory nerve fibers of aged gerbils raised in quiet or noise

    Hear. Res.

    (1990)
  • B.A. Schulte et al.

    Lateral wall Na,K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils

    Hear. Res.

    (1992)
  • S.S. Spicer et al.

    Expression patterns of ion transport enzymes in spiral ligament fibrocytes change in relation to strial atrophy in the aged gerbil cochlear

    Hear. Res.

    (1997)
  • K.D. Statler et al.

    Development of mature microcystic lesions in the cochlear nuclei of the Mongolian gerbil

    Hear. Res.

    (1990)
  • Q.Y. Zheng et al.

    Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses

    Hear. Res.

    (1999)
  • E. Borg et al.

    Hearing thresholds in the rabbit. A behavioral and electrophysiological study

    Acta Otolaryngol.

    (1983)
  • M.L. Cheal

    The gerbil: A unique model for research on aging

    Exp. Aging Res.

    (1986)
  • W.A. Cooper et al.

    Auditory brainstem responses to tonal stimuli in young and aging rat

    Hear. Res.

    (1990)
  • K.J. Cruickshanks et al.

    Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study

    Am. J. Epidemiol.

    (1998)
  • A. Czibulka et al.

    Neuronal populations in the gerbil PVCN: Effects of age, hearing status and microcysts

    Hear. Res.

    (1991)
  • A.C. Davis

    The prevalence of hearing impairment and reported hearing disability among adults in Great Britain

    Int. J. Epidemiol.

    (1989)
  • A.C. Davis

    Epidemiological profile of hearing impairments: the scale and nature of the problem with special reference to elderly

    Acta Otolaryngol. Suppl.

    (1990)
  • Davis, A.C., 1997. Epidemiology. In: Stephens, D. (Ed.), Scott-Brown’s Otolaryngology, Sixth edition (General Editor:...
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