ABSTRACT
In order to examine auditory thresholds and hearing sensitivity during aging in the gray mouse lemur (Microcebus murinus), suggested to represent a model for early primate evolution and Alzheimer research, we applied brainstem-evoked response audiometry (BERA), traditionally used for screening hearing sensitivity in human babies. To assess the effect of age, we determined auditory thresholds in two age groups of adult mouse lemurs (young adults, 1–5 years; old adults, ≥7 years) using clicks and tone pips. Auditory thresholds indicated frequency sensitivity from 800 Hz to almost 50 kHz, covering the species tonal communication range with fundamentals from about 8 to 40 kHz. The frequency of best hearing at 7.9 kHz was slightly lower than that and coincided with the dominant frequencies of communication signals of a predator. Aging shifted auditory thresholds in the range between 2 and 50.4 kHz significantly by 12–27 dB. This mild presbyacusis, expressed in a drop of amplitudes of BERA signals, but not discernible in latencies of responses, suggests a metabolic age-related decrease potentially combined with an accompanying degeneration of the cochlear nerve. Our findings on hearing range of this species support the hypothesis that predation was a driving factor for the evolution of hearing in small ancestral primates. Likewise, results provide the empirical basis for future approaches trying to differentiate peripheral from central factors when studying Alzheimer’s disease-like pathologies in the aging brain.
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Abbreviations
- AD:
-
Alzheimer’s disease
- ARHL:
-
age-related hearing loss
- ABR:
-
auditory brainstem response
- BERA:
-
brainstem-evoked response audiometry
- EP:
-
endocochlear potential
- SPL:
-
sound pressure level
REFERENCES
Alegre M, Gurtubay IG, Iriarte J, Ciordia E, Manrique M, Artieda J (2001) Brainstem auditory evoked potentials (BAEPs) in the cynomolgus macaque monkey: equivalence with human BAEPs and proposal of a new nomenclature. Hear Res 151:115–120
Biacabe B, Chevallier JM, Avan P, Bonfils P (2001) Functional anatomy of auditory brainstem nuclei: application to the anatomical basis of brainstem auditory evoked potentials. Auris Nasus Larynx 28:85–94
Boettcher FA (2002) Presbyacusis and the auditory brainstem response. J Speech Lang Hear Res 45:1249–1261
Boettcher FA, Mills JH, Norton BL (1993a) Age-related changes in auditory evoked potentials of gerbils. I. Response amplitudes. Hear Res 71:137–145
Boettcher FA, Mills JH, Norton BL, Schmiedt RA (1993b) Age-related changes in auditory evoked potentials of gerbils. II. Response latencies. Hear Res 71:146–156
Bons N, Mestre N, Petter A (1992) Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiol Aging 13:99–105
Bons N, Jallageas V, Silhol S, Mestre-Frances N, Petter A, Delacourte A (1995) Immunocytochemical characterization of Tau proteins during cerebral aging of the lemurian primate Microcebus murinus. C R Acad Sci III 318:77–83
Bons N, Rieger F, Prudhomme D, Fisher A, Krause KH (2006) Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer’s disease? Genes Brain Behav 5:120–30
Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308
Bunkus E, Scheumann M, Zimmermann E (2005) Does acoustic predator recognition require experience in ancient primates? 29th International Ethological Conference. Budapest 20.–27(8):39
CHABA (1988) Speech understanding and aging. J Acoust Soc Am 83:859–820
Chabert R (1998) Protocoles d’exploration neurofonctionnelle du système auditif et de l’activité faciale. PhD thesis, Ecole pratique des hautes études, Paris
Chen B, Zhong Y, Peng W, Sun Y, Kong W-J (2010) Age-related changes in the central auditory system: comparison of d-galactose-induced aging rats and naturally aging rats. Brain Res 1344:43–53
Chisolm TH, Willott JF, Lister JJ (2003) The aging auditory system: anatomic and physiologic changes and implications for rehabilitation. Int J Audiol 42:2S3–10
Coleman M (2009) What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int J Primatol 30:55–91
Delacourte A, Sautiere PE, Wattez A, Mourton-Gilles C, Petter A, Bons N (1995) Biochemical characterization of Tau proteins during cerebral aging of the lemurian primate Microcebus murinus. C R Acad Sci III 318:85–9
Dhenain M, Michot JL, Privat N, Picq JL, Boller F, Duyckaerts C, Volk A (2000) MRI description of cerebral atrophy in mouse lemur primates. Neurobiol Aging 21:81–8
Dubno JR, Eckert MA, Lee FS, Matthews LJ, Schmiedt RA (2013) Classifying human audiometric phenotypes of age-related hearing loss from animal models. J Assoc Res Otolaryngol 14:687–701
Fichtel C, Kappeler PM (2002) Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav Ecol Sociobiol 51:262–275
Fischer KE, Austad SN (2011) The development of small primate models for aging research. ILAR J 52:78–88
Goerlitz HR, Siemers BM (2007) Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Funct Ecol 21:143–153
Gordon-Salant S, Frisina RD (2010) Introduction and overview. In: Gordon-Salant S, Frisina RD, Popper AN, Fay RR (eds) The aging auditory system. Springer, New York, pp 1–8
Haccou P, Meelis E (1994) Statistical analysis of behavioural data. Oxford University Press, New York
Heffner RS (2004) Primate hearing from a mammalian perspective. Anat Rec A: Discov Mol Cell Evol Biol 281:1111–1122
Henry KR (1982) Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J Gerontol 37:275–282
Henry KR, McGinn MD, Chole RA (1980) Age-related auditory loss in the Mongolian gerbil. Eur Arch Otorhinolaryngol 228:233–238
Humes LE, Dubno JR, Gordon-Salant S, Lister JJ, Cacace AT, Cruickshanks KJ, Gates GA, Wilson RH, Wingfield A (2012) Central presbycusis: a review and evaluation of the evidence. J Am Acad Audiol 23:635–666
Ingham NJ, Thornton SK, Comis SD, Withington DJ (1998) The auditory brainstem response of aged guinea pigs. Acta Otolaryngol 118:673–680
Ison JR, Tremblay KL, Allen PD (2010) Closing the gap between neurobiology and human presbycusis: behavioral and evoked potential studies of age-related hearing loss in animal models and in humans. In: Gordon-Salant S, Frisina RD, Popper AN, Fay RR (eds) The aging auditory system. Springer, New York, pp 75–110
Joly M, Ammersdörfer S, Craul M, Schmidtke D, Zimmermann E (2013) A touch-screen cognitive testing method for an emerging primate brain aging model, the mouse lemur (Microcebus murinus). Paper presented at the 10th Göttingen Meeting of the German Neuroscience Society, Göttingen
Kappel P, Hohenbrink S, Radespiel U (2011) Experimental evidence for olfactory predator recognition in wild mouse lemurs. Am J Primatol 73:928–938
Kessler SE, Radespiel U, Hasiniaina AI, Leliveld LM, Nash LT, Zimmermann E (2014) Modeling the origins of mammalian sociality: moderate evidence for matrilineal signatures in mouse lemur vocalizations. Front Zool 11:14
Kraska A, Dorieux O, Picq JL et al (2011) Age-associated cerebral atrophy in mouse lemur primates. Neurobiol Aging 32:894–906
Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085
Leliveld LMC, Scheumann M, Zimmermann E (2011) Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus). J Acoust Soc Am 129:2278–2288
Lin FR, Metter EJ, O’Brien RJ, Resnick SM, Zonderman AB, Ferrucci L (2011a) Hearing loss and incident dementia. Arch Neurol 68:214–220
Lin H, Furman A, Kujawa S, Liberman MC (2011b) Primary neural degeneration in the guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12:605–616
Lindenberger U, Baltes PB (1949) Sensory functioning and intelligence in old age: a strong connection. Psychol Aging 9:339–355
Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philos Trans R Soc Lond B Biol Sci 264:295–352
Martin RD (1995) Prosimians: from obscurity to extinction? In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 535–563
Mazelová J, Popelar J, Syka J (2003) Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 38:87–94
McFadden SL, Campo P, Quaranta N, Henderson D (1997) Age-related decline of auditory function in the chinchilla (Chinchilla laniger). Hear Res 111:114–126
Melcher JR, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat III: identified cell populations. Hear Res 93:52–71
Melcher JR, Knudson IM, Fullerton BC, Guinan JJ Jr, Norris BE, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat. I. An experimental approach to their identification. Hear Res 93:1–27
Mestre-Francés N, Keller E, Calenda A, Barelli H, Checler F, Bons N (2000) Immunohistochemical analysis of cerebral cortical and vascular lesions in the primate Microcebus murinus reveal distinct amyloid beta1-42 and beta1-40 immunoreactivity profiles. Neurobiol Dis 7:1–8
Mitchell C, Vernon J, Herman P (1971) What does the lemur really hear? J Acoust Soc Am 50:710–711
Møller AR (2006) Hearing: anatomy, physiology, and disorders of the auditory system, 2nd edn. Academic, San Diego
Nemoz-Bertholet F, Aujard F (2003) Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Exp Gerontol 38:407–414
Niaussat MM, Petter JJ (1980) Etude de la sensibilité auditive d’un Lemurien malgache : Microcebus murinus (J.-F. Miller, 1777). Mammalia 44:553–558
Ohlemiller KK (2004) Age-related hearing loss: the status of Schuknecht’s typology. Curr Opin Otolaryngol 12:439–443
Osmanski MS, Wang X (2011) Measurement of absolute auditory thresholds in the common marmoset (Callithrix jacchus). Hear Res 277:127–133
Perret M (1995) Chemocommunication in the reproductive function of mouse lemurs. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 377–392
Piep M, Radespiel U, Zimmermann E, Schmidt S, Siemers BM (2008) The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus. Anim Behav 75:871–878
Pleis J, Lethbridge-Çejku M (2007) Summary health statistics for U.S. adults: National Health Interview Survey, 2006. National Center for Health Statistics, Vital Health Stat 10(235) US Government Printing Office., Washington, DC
Rahlfs M, Fichtel C (2010) Anti-predator behaviour in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Ethology 116:429–439
Ramsier MA, Dominy NJ (2010) A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang. Am J Primatol 72:217–233
Ramsier MA, Dominy NJ (2012) Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis). Commun Integr Biol 5:637–40
Ramsier MA, Cunningham AJ, Finneran JJ, Dominy NJ (2012a) Social drive and the evolution of primate hearing. Philos Trans R Soc Lond B Biol Sci 367:1860–1868
Ramsier MA, Cunningham AJ, Moritz GL, Finneran JJ, Williams CV, Ong PS, Gursky-Doyen SL, Dominy NJ (2012b) Primate communication in the pure ultrasound. Biol Lett 8:508–511
Sand T (1991) BAEP amplitudes and amplitude ratios: relation to click polarity, rate, age and sex. Electroen Clin Neuro 78:291–296
Schehka S, Esser KH, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). J Comp Physiol A 193:845–852
Scheumann M, Rabesandratana A, Zimmermann E (2007) Predation, communication, and cognition in lemurs. In: Gursky SL, Nekaris KAI (eds) Primate anti-predator strategies. Developments in primatology: progress and prospects. Springer, New York, pp 100–126
Schmiedt RA (2010) The physiology of cochlear presbycusis. In: Gordon-Salant S, Frisina RD, Fay RR, Popper A (eds) The aging auditory system. Springer, New York, pp 9–38
Schuknecht HF (1974) Pathology of the ear, 1st edn. Harvard University Press, Cambridge
Sekuler R, Blake R (1987) Sensory underload. Psychol Today 21:48–51
Siemers BM, Goerlitz HR, Robsomanitrandrasana E, Piep M, Ramanamanjato J-B, Rakotondravony D, Ramilijaona O, Ganzhorn JU (2007) Sensory basis of food detection in wild Microcebus murinus. Int J Primatol 28:291–304
Sündermann D, Scheumann M, Zimmermann E (2008) Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus). J Comp Psychol 122:146–155
Tillein J, Heid S, Lang E, Hartmann R, Kral A (2012) Development of brainstem-evoked responses in congenital auditory deprivation. Neural Plast 2012:182767
Torre P III, Fowler CG (2000) Age-related changes in auditory function of rhesus monkeys (Macaca mulatta). Hear Res 142:131–140
Trouche SG, Maurice T, Rouland S, Verdier JM, Mestre-Francés N (2010) The three-panel runway maze adapted to Microcebus murinus reveals age-related differences in memory and perseverance performances. Neurobiol Learn Mem 94:100–106
Valentijn SA, van Boxtel MP, van Hooren SA, Bosma H, Beckers HJ, Ponds RW, Jolles J (2005) Change in sensory functioning predicts change in cognitive functioning: results from a 6-year follow-up in the maastricht aging study. J Am Geriatr Soc 53:374–380
Weigl R (2005) Longevity of mammals in captivity; from the living collections of the world. Schweizerbart Science Publishers
Willott JF, Schacht J (2010) Interventions and future therapies: lessons from animal models. In: Gordon-Salant S, Frisina RD, Fay RR, Popper A (eds) The aging auditory system. Springer, New York, pp 275–293
Wrogemann D, Radespiel U, Zimmermann E (2001) Comparison of reproductive characteristics and changes in body weight between captive populations of rufous and gray mouse lemurs. Int J Primatol 22:91–108
Zimmermann E (2010) Vocal expression of emotion in a nocturnal prosimian primate group, mouse lemurs. In: Brudzynski SM (ed) Handbook of mammalian vocalization: an integrative neuroscience approach. Academic, Oxford, pp 215–226
ACKNOWLEDGMENTS
We would like to thank F. Sherwood-Brock for checking the English in the manuscript, H.-J. Sauer, L. Müller, and K. Nitschke for animal care and S. von den Berg and K.-H. Esser for technical support. This study was financially supported by a Georg-Christoph-Lichtenberg scholarship (CS) and in part by the DFG Cluster of Excellence Hearing4all (PH and AK) and the European Community’s 7th Framework Programme (FP7/2007-2013) under grant agreement no. 278486 acronym “DEVELAGE” (EZ).
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The authors declare no actual or potential conflicts of interest.
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Christian Schopf, Elke Zimmermann, and Andrej Kral are contributed equally to the study.
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Schopf, C., Zimmermann, E., Tünsmeyer, J. et al. Hearing and Age-Related Changes in the Gray Mouse Lemur. JARO 15, 993–1005 (2014). https://doi.org/10.1007/s10162-014-0478-4
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DOI: https://doi.org/10.1007/s10162-014-0478-4