Skip to main content
Top
Published in: Journal of the Association for Research in Otolaryngology 6/2014

01-12-2014 | Research Article

Hearing and Age-Related Changes in the Gray Mouse Lemur

Authors: Christian Schopf, Elke Zimmermann, Julia Tünsmeyer, Sabine B. R. Kästner, Peter Hubka, Andrej Kral

Published in: Journal of the Association for Research in Otolaryngology | Issue 6/2014

Login to get access

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.
Literature
go back to reference 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 151:115–120PubMedCrossRef 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 151:115–120PubMedCrossRef
go back to reference 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 28:85–94PubMedCrossRef 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 28:85–94PubMedCrossRef
go back to reference Boettcher FA (2002) Presbyacusis and the auditory brainstem response. J Speech Lang Hear Res 45:1249–1261PubMedCrossRef Boettcher FA (2002) Presbyacusis and the auditory brainstem response. J Speech Lang Hear Res 45:1249–1261PubMedCrossRef
go back to reference Boettcher FA, Mills JH, Norton BL (1993a) Age-related changes in auditory evoked potentials of gerbils. I. Response amplitudes. Hear Res 71:137–145PubMedCrossRef Boettcher FA, Mills JH, Norton BL (1993a) Age-related changes in auditory evoked potentials of gerbils. I. Response amplitudes. Hear Res 71:137–145PubMedCrossRef
go back to reference Boettcher FA, Mills JH, Norton BL, Schmiedt RA (1993b) Age-related changes in auditory evoked potentials of gerbils. II. Response latencies. Hear Res 71:146–156PubMedCrossRef Boettcher FA, Mills JH, Norton BL, Schmiedt RA (1993b) Age-related changes in auditory evoked potentials of gerbils. II. Response latencies. Hear Res 71:146–156PubMedCrossRef
go back to reference Bons N, Mestre N, Petter A (1992) Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiol Aging 13:99–105PubMedCrossRef Bons N, Mestre N, Petter A (1992) Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiol Aging 13:99–105PubMedCrossRef
go back to reference 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 318:77–83PubMed 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 318:77–83PubMed
go back to reference 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 5:120–30PubMedCrossRef 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 5:120–30PubMedCrossRef
go back to reference Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308CrossRef Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308CrossRef
go back to reference 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 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
go back to reference Chabert R (1998) Protocoles d’exploration neurofonctionnelle du système auditif et de l’activité faciale. PhD thesis, Ecole pratique des hautes études, Paris Chabert R (1998) Protocoles d’exploration neurofonctionnelle du système auditif et de l’activité faciale. PhD thesis, Ecole pratique des hautes études, Paris
go back to reference 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 1344:43–53PubMedCrossRef 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 1344:43–53PubMedCrossRef
go back to reference Chisolm TH, Willott JF, Lister JJ (2003) The aging auditory system: anatomic and physiologic changes and implications for rehabilitation. Int J Audiol 42:2S3–10PubMedCrossRef Chisolm TH, Willott JF, Lister JJ (2003) The aging auditory system: anatomic and physiologic changes and implications for rehabilitation. Int J Audiol 42:2S3–10PubMedCrossRef
go back to reference Coleman M (2009) What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int J Primatol 30:55–91CrossRef Coleman M (2009) What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int J Primatol 30:55–91CrossRef
go back to reference 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 318:85–9PubMed 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 318:85–9PubMed
go back to reference 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 21:81–8PubMedCrossRef 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 21:81–8PubMedCrossRef
go back to reference 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 14:687–701PubMedCentralPubMedCrossRef 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 14:687–701PubMedCentralPubMedCrossRef
go back to reference Fichtel C, Kappeler PM (2002) Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav Ecol Sociobiol 51:262–275CrossRef Fichtel C, Kappeler PM (2002) Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav Ecol Sociobiol 51:262–275CrossRef
go back to reference Fischer KE, Austad SN (2011) The development of small primate models for aging research. ILAR J 52:78–88PubMedCrossRef Fischer KE, Austad SN (2011) The development of small primate models for aging research. ILAR J 52:78–88PubMedCrossRef
go back to reference Goerlitz HR, Siemers BM (2007) Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Funct Ecol 21:143–153CrossRef Goerlitz HR, Siemers BM (2007) Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Funct Ecol 21:143–153CrossRef
go back to reference 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 1–8CrossRef 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 1–8CrossRef
go back to reference Haccou P, Meelis E (1994) Statistical analysis of behavioural data. Oxford University Press, New York Haccou P, Meelis E (1994) Statistical analysis of behavioural data. Oxford University Press, New York
go back to reference Heffner RS (2004) Primate hearing from a mammalian perspective. Anat Rec A: Discov Mol Cell Evol Biol 281:1111–1122CrossRef Heffner RS (2004) Primate hearing from a mammalian perspective. Anat Rec A: Discov Mol Cell Evol Biol 281:1111–1122CrossRef
go back to reference Henry KR (1982) Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J Gerontol 37:275–282PubMedCrossRef Henry KR (1982) Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J Gerontol 37:275–282PubMedCrossRef
go back to reference Henry KR, McGinn MD, Chole RA (1980) Age-related auditory loss in the Mongolian gerbil. Eur Arch Otorhinolaryngol 228:233–238CrossRef Henry KR, McGinn MD, Chole RA (1980) Age-related auditory loss in the Mongolian gerbil. Eur Arch Otorhinolaryngol 228:233–238CrossRef
go back to reference 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 23:635–666PubMedCrossRef 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 23:635–666PubMedCrossRef
go back to reference Ingham NJ, Thornton SK, Comis SD, Withington DJ (1998) The auditory brainstem response of aged guinea pigs. Acta Otolaryngol 118:673–680PubMedCrossRef Ingham NJ, Thornton SK, Comis SD, Withington DJ (1998) The auditory brainstem response of aged guinea pigs. Acta Otolaryngol 118:673–680PubMedCrossRef
go back to reference 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 75–110CrossRef 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 75–110CrossRef
go back to reference 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 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
go back to reference Kappel P, Hohenbrink S, Radespiel U (2011) Experimental evidence for olfactory predator recognition in wild mouse lemurs. Am J Primatol 73:928–938PubMedCrossRef Kappel P, Hohenbrink S, Radespiel U (2011) Experimental evidence for olfactory predator recognition in wild mouse lemurs. Am J Primatol 73:928–938PubMedCrossRef
go back to reference 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 11:14PubMedCentralPubMedCrossRef 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 11:14PubMedCentralPubMedCrossRef
go back to reference Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085PubMedCentralPubMedCrossRef Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085PubMedCentralPubMedCrossRef
go back to reference 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 129:2278–2288PubMedCrossRef 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 129:2278–2288PubMedCrossRef
go back to reference Lin FR, Metter EJ, O’Brien RJ, Resnick SM, Zonderman AB, Ferrucci L (2011a) Hearing loss and incident dementia. Arch Neurol 68:214–220PubMedCentralPubMed Lin FR, Metter EJ, O’Brien RJ, Resnick SM, Zonderman AB, Ferrucci L (2011a) Hearing loss and incident dementia. Arch Neurol 68:214–220PubMedCentralPubMed
go back to reference 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 12:605–616PubMedCentralPubMedCrossRef 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 12:605–616PubMedCentralPubMedCrossRef
go back to reference Lindenberger U, Baltes PB (1949) Sensory functioning and intelligence in old age: a strong connection. Psychol Aging 9:339–355CrossRef Lindenberger U, Baltes PB (1949) Sensory functioning and intelligence in old age: a strong connection. Psychol Aging 9:339–355CrossRef
go back to reference Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philos Trans R Soc Lond B Biol Sci 264:295–352PubMedCrossRef Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philos Trans R Soc Lond B Biol Sci 264:295–352PubMedCrossRef
go back to reference 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 535–563CrossRef 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 535–563CrossRef
go back to reference Mazelová J, Popelar J, Syka J (2003) Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 38:87–94PubMedCrossRef Mazelová J, Popelar J, Syka J (2003) Auditory function in presbycusis: peripheral vs. central changes. Exp Gerontol 38:87–94PubMedCrossRef
go back to reference McFadden SL, Campo P, Quaranta N, Henderson D (1997) Age-related decline of auditory function in the chinchilla (Chinchilla laniger). Hear Res 111:114–126PubMedCrossRef McFadden SL, Campo P, Quaranta N, Henderson D (1997) Age-related decline of auditory function in the chinchilla (Chinchilla laniger). Hear Res 111:114–126PubMedCrossRef
go back to reference Melcher JR, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat III: identified cell populations. Hear Res 93:52–71PubMedCrossRef Melcher JR, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat III: identified cell populations. Hear Res 93:52–71PubMedCrossRef
go back to reference 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 93:1–27PubMedCrossRef 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 93:1–27PubMedCrossRef
go back to reference 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 7:1–8PubMedCrossRef 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 7:1–8PubMedCrossRef
go back to reference Mitchell C, Vernon J, Herman P (1971) What does the lemur really hear? J Acoust Soc Am 50:710–711PubMedCrossRef Mitchell C, Vernon J, Herman P (1971) What does the lemur really hear? J Acoust Soc Am 50:710–711PubMedCrossRef
go back to reference Møller AR (2006) Hearing: anatomy, physiology, and disorders of the auditory system, 2nd edn. Academic, San Diego Møller AR (2006) Hearing: anatomy, physiology, and disorders of the auditory system, 2nd edn. Academic, San Diego
go back to reference Nemoz-Bertholet F, Aujard F (2003) Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Exp Gerontol 38:407–414PubMedCrossRef Nemoz-Bertholet F, Aujard F (2003) Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Exp Gerontol 38:407–414PubMedCrossRef
go back to reference Niaussat MM, Petter JJ (1980) Etude de la sensibilité auditive d’un Lemurien malgache : Microcebus murinus (J.-F. Miller, 1777). Mammalia 44:553–558CrossRef Niaussat MM, Petter JJ (1980) Etude de la sensibilité auditive d’un Lemurien malgache : Microcebus murinus (J.-F. Miller, 1777). Mammalia 44:553–558CrossRef
go back to reference Ohlemiller KK (2004) Age-related hearing loss: the status of Schuknecht’s typology. Curr Opin Otolaryngol 12:439–443CrossRef Ohlemiller KK (2004) Age-related hearing loss: the status of Schuknecht’s typology. Curr Opin Otolaryngol 12:439–443CrossRef
go back to reference 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 377–392CrossRef 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 377–392CrossRef
go back to reference 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 75:871–878CrossRef 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 75:871–878CrossRef
go back to reference 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 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
go back to reference Rahlfs M, Fichtel C (2010) Anti-predator behaviour in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Ethology 116:429–439CrossRef Rahlfs M, Fichtel C (2010) Anti-predator behaviour in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Ethology 116:429–439CrossRef
go back to reference 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 72:217–233PubMedCrossRef 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 72:217–233PubMedCrossRef
go back to reference 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 367:1860–1868PubMedCentralPubMedCrossRef 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 367:1860–1868PubMedCentralPubMedCrossRef
go back to reference 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 8:508–511PubMedCentralPubMedCrossRef 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 8:508–511PubMedCentralPubMedCrossRef
go back to reference Sand T (1991) BAEP amplitudes and amplitude ratios: relation to click polarity, rate, age and sex. Electroen Clin Neuro 78:291–296CrossRef Sand T (1991) BAEP amplitudes and amplitude ratios: relation to click polarity, rate, age and sex. Electroen Clin Neuro 78:291–296CrossRef
go back to reference Schehka S, Esser KH, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). J Comp Physiol A 193:845–852CrossRef Schehka S, Esser KH, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). J Comp Physiol A 193:845–852CrossRef
go back to reference 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 100–126CrossRef 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 100–126CrossRef
go back to reference 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 9–38CrossRef 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 9–38CrossRef
go back to reference Schuknecht HF (1974) Pathology of the ear, 1st edn. Harvard University Press, Cambridge Schuknecht HF (1974) Pathology of the ear, 1st edn. Harvard University Press, Cambridge
go back to reference Sekuler R, Blake R (1987) Sensory underload. Psychol Today 21:48–51 Sekuler R, Blake R (1987) Sensory underload. Psychol Today 21:48–51
go back to reference 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 28:291–304CrossRef 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 28:291–304CrossRef
go back to reference Sündermann D, Scheumann M, Zimmermann E (2008) Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus). J Comp Psychol 122:146–155PubMedCrossRef Sündermann D, Scheumann M, Zimmermann E (2008) Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus). J Comp Psychol 122:146–155PubMedCrossRef
go back to reference Tillein J, Heid S, Lang E, Hartmann R, Kral A (2012) Development of brainstem-evoked responses in congenital auditory deprivation. Neural Plast 2012:182767PubMedCentralPubMed Tillein J, Heid S, Lang E, Hartmann R, Kral A (2012) Development of brainstem-evoked responses in congenital auditory deprivation. Neural Plast 2012:182767PubMedCentralPubMed
go back to reference Torre P III, Fowler CG (2000) Age-related changes in auditory function of rhesus monkeys (Macaca mulatta). Hear Res 142:131–140PubMedCrossRef Torre P III, Fowler CG (2000) Age-related changes in auditory function of rhesus monkeys (Macaca mulatta). Hear Res 142:131–140PubMedCrossRef
go back to reference 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 94:100–106PubMedCentralPubMedCrossRef 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 94:100–106PubMedCentralPubMedCrossRef
go back to reference 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 53:374–380PubMedCrossRef 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 53:374–380PubMedCrossRef
go back to reference Weigl R (2005) Longevity of mammals in captivity; from the living collections of the world. Schweizerbart Science Publishers Weigl R (2005) Longevity of mammals in captivity; from the living collections of the world. Schweizerbart Science Publishers
go back to reference 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 275–293CrossRef 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 275–293CrossRef
go back to reference 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 22:91–108CrossRef 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 22:91–108CrossRef
go back to reference 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 215–226CrossRef 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 215–226CrossRef
Metadata
Title
Hearing and Age-Related Changes in the Gray Mouse Lemur
Authors
Christian Schopf
Elke Zimmermann
Julia Tünsmeyer
Sabine B. R. Kästner
Peter Hubka
Andrej Kral
Publication date
01-12-2014
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 6/2014
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-014-0478-4

Other articles of this Issue 6/2014

Journal of the Association for Research in Otolaryngology 6/2014 Go to the issue