Skip to main content

Hearing and Vocalizations in the Naked Mole-Rat

  • Chapter
  • First Online:
Book cover The Extraordinary Biology of the Naked Mole-Rat

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1319))

Abstract

Since their discovery, naked mole-rats have been speaking to us. Early field studies noted their extensive vocalizations, and scientists who are fortunate enough to spend time with these creatures in the laboratory setting cannot help but notice their constant peeping, chirruping and grunting (Hill et al., Proc Zool Soc Lond 128:455–514, 1957). Yet, few dwell on the function of these chirps and peeps, being instead drawn to the many other extraordinary aspects of naked mole-rat physiology detailed throughout this book. Still, no biology is complete without a description of how an organism communicates. While the field of naked mole-rat bioacoustics and acoustic communication has been largely silent for many years, we highlight recent progress in understanding how and what Heterocephalus glaber hears and which vocalizations it uses. These efforts are essential for a complete understanding of naked mole-rat cooperation, society and even culture.

figure a

Photo Credit: Thomas Park

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABR:

auditory brainstem response

AC:

auditory cortex

AVCN:

anterior ventral cochlear nucleus

BK channel:

big potassium channel

CN:

cochlear nucleus

DCN:

dorsal cochlear nucleus

DNLL:

dorsal nucleus of the lateral lemniscus

GluR:

glutamate receptor

GlyT2:

glycine transporter 2

HCN1:

Hyperpolarization-activated cyclic nucleotide-gated channel 1

HM:

head of malleus

IC:

inferior colliculus

IHC:

inner hair cells

KV1.1:

Potassium voltage-gated channel subfamily A member 1

LPI:

long process of the incus

LSO:

lateral superior olive

MGN:

medial geniculate nucleus

MM:

manubrium of malleus

MNTB:

medial nucleus of the trapezoid body

mPFC:

medial prefrontal cortex

MSO:

medial superior olive

Na,K-ATPase α3:

sodium/potassium-ATPase (Na+/K+-ATPase)

OHC:

outer hair cells

PVCN:

posterior ventral cochlear nucleus

SGN:

spiral ganglion neurons

SOC:

superior olivary complex

SPI:

short process of the incus

TM:

tympanic membrane

TT:

tensor tympani tendon

VCN:

ventral cochlear nucleus

vGluT1:

vesicular glutamate transporter 1

VNLL:

ventral nucleus of the lateral lemniscus

References

  • Aitkin LM, Horseman BG, Bush BM (1982) Some aspects of the auditory pathway and audition in the European mole, Talpa europaea. Brain Behav Evol 21:49–59

    Google Scholar 

  • Altieri SC, Zhao T, Jalabi W, Maricich SM (2014) Development of glycinergic innervation to the murine LSO and SPN in the presence and absence of the MNTB. Front Neural Circuits 8:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Arriaga G, Zhou EP, Jarvis ED (2012) Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One 7:e46610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashmore J, Avan P, Brownell WE, Dallos P, Dierkes K, Fettiplace R, Grosh K, Hackney CM, Hudspeth AJ, Julicher F (2010) The remarkable cochlear amplifier. Hear Res 266:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker AJ, Veviurko G, Bennett NC, Hart DW, Mograby L, Lewin GR (2021) Cultural transmission of vocal dialect in the naked mole-rat. Science 371(6528):503–507

    Google Scholar 

  • Barone CM, Douma S, Reijntjes DOJ, Browe BM, Koppl C, Klump G, Park TJ, Pyott SJ (2019) Altered cochlear innervation in developing and mature naked and Damaraland mole rats. J Comp Neurol 527(14):2302–2316

    Google Scholar 

  • Bednářová R, Hrouzková-Knotková E, Burda H, Sedláček F, Šumbera R (2013) Vocalizations of the giant mole-rat (Fukomys mechowii), a subterranean rodent with the richest vocal repertoire. Bioacoustics 22:87–107

    Google Scholar 

  • Begall S, Burda H, Schneider B (2004) Hearing in coruros (Spalacopus cyanus): special audiogram features of a subterranean rodent. J Comp Physiol Neuroethol Sens Neural Behav Physiol 190:963–969

    Google Scholar 

  • Bennett NC, Faulkes C (2000) African Mole-Rats: Ecology and Eusociality | zoology. Cambridge University Press

    Google Scholar 

  • Bennett NC, Jarvis JUM (1988) The reproductive biology of the Cape mole-rat, Georychus capensis (Rodentia, Bathyergidae). J Zool 214:95–106

    Google Scholar 

  • Billups B (2005) Colocalization of vesicular glutamate transporters in the rat superior olivary complex. Neurosci Lett 382:66–70

    Article  CAS  PubMed  Google Scholar 

  • Borst JGG, Soria van Hoeve J (2012) The Calyx of held synapse: from model synapse to auditory relay. Annu Rev Physiol 74:199–224

    Article  CAS  PubMed  Google Scholar 

  • Bouchet H, Blois-Heulin C, Lemasson A (2013) Social complexity parallels vocal complexity: a comparison of three non-human primate species. Front Psychol 4:390

    Google Scholar 

  • Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–547

    Article  CAS  PubMed  Google Scholar 

  • Brett RA (1991) The ecology of naked mole-rat colonies: burrowing, food, and limiting factors. In: The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 137-184

    Google Scholar 

  • Bronchti G, Heil P, Scheich H, Wollberg Z (1989) Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. 2-deoxyglucose study of subcortical centers. J Comp Neurol 284:253–274

    Google Scholar 

  • Brückmann G, Burda H (1997) Hearing in blind subterranean Zambian mole-rats (Cryptomys sp.): collective behavioural audiogram in a highly social rodent. J Comp Physiol A 181:83–88

    Google Scholar 

  • Bruns V, Müller M, Hofer W, Heth G, Nevo E (1988) Inner ear structure and electrophysiological audiograms of the subterranean mole rat, Spalax ehrenbergi. Hear Res 33:1–9

    Google Scholar 

  • Buffenstein R, Craft W (2021) The idiosyncratic physiological traits of the naked mole-rat; a resilient animal model of aging, longevity, and healthspan. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 221–254

    Google Scholar 

  • Buffenstein R, Yahav S (1991) Is the naked mole-rat Heterocephalus glaber an endothermic yet poikilothermic mammal? J Thermal Biol 16(4):227–232

    Google Scholar 

  • Clarke FM, Faulkes CG (1997) Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber. Proc R Soc Lond B Biol Sci 264:993–1000

    Google Scholar 

  • Coen CW, Bennett NC, Holmes MM, Faulkes CG (2021) Neuropeptidergic and neuroendocrine systems underlying eusociality and the concomitant social regulation of reproduction in naked mole-rats: a comparative approach. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 59–103

    Google Scholar 

  • Credner S, Burda H, Ludescher F (1997) Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae). J Comp Physiol A 180:245–255

    Google Scholar 

  • Darrow KN, Maison SF, Liberman MC (2006) Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9:1474–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dent ML, Screven LA, Kobrina A (2018) Hearing in rodents. In: Dent ML, Fay RR, Popper AN (eds) Rodent Bioacoustics. Springer, Cham, pp 71–105

    Chapter  Google Scholar 

  • Dunbar R (1998) The social brain hypothesis. Evol Anthropol 6:178–190

    Article  Google Scholar 

  • Edrey YH, Hanes M, Pinto M, Mele J, Buffenstein R (2011) Successful aging and sustained good health in the naked mole rat: a long-lived mammalian model for biogerontology and biomedical research. ILAR J 52:41–53

    Article  CAS  PubMed  Google Scholar 

  • Ehret G (1976) Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1:179–184

    Google Scholar 

  • Ehret G, Frankenreiter M (1977) Quantitative analysis of cochlear structures in the house mouse in relation to mechanisms of acoustical information processing. J Comp Neurol 122:65–85

    Google Scholar 

  • Eybalin M, Caicedo A, Renard N, Ruel J, Puel JL (2004) Transient Ca2+−permeable AMPA receptors in postnatal rat primary auditory neurons. Eur J Neurosci 20:2981–2989

    Article  PubMed  Google Scholar 

  • Faulkes CG, Bennet NC (2021) Social evolution in African mole-rats – a comparative overview. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 1–33

    Google Scholar 

  • Finck A, Schneck CD, Hartman AF (1972) Development of cochlear function in the neonate Mongolian gerbil (Meriones unguiculatus). J Comp Physiol Psychol 78:375–380

    Google Scholar 

  • Fischer J, Farnworth MS, Sennhenn-Reulen H, Hammerschmidt K (2017) Quantifying social complexity. Anim Behav 130:57–66

    Article  Google Scholar 

  • Fischer J, Hammerschmidt K, Cheney DL, Seyfarth RM (2002) Acoustic features of male baboon loud calls: influences of context, age, and individuality. J Acoust Soc Am 111:1465–1474

    Article  PubMed  Google Scholar 

  • Freeberg TM, Krams I (2015) Does social complexity link vocal complexity and cooperation? J Ornithol 156:125–132

    Article  Google Scholar 

  • Friauf E, Aragón C, Löhrke S, Westenfelder B, Zafra F (1999) Developmental expression of the glycine transporter GLYT2 in the auditory system of rats suggests involvement in synapse maturation. J Comp Neurol 412:17–37

    Article  CAS  PubMed  Google Scholar 

  • Geal-Dor M, Freeman S, Li G, Sohmer H (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res 69:236–242

    Article  CAS  PubMed  Google Scholar 

  • Gerhardt P, Henning Y, Begall S, Malkemper EP (2017) Audiograms of three subterranean rodent species (genus Fukomys) determined by auditory brainstem responses reveal extremely poor high-frequency cut-offs. J Exp Biol 220:4377–4382

    Google Scholar 

  • Gessele N, Garcia-Pino E, Omerbašić D, Park TJ, Koch U (2016) Structural changes and lack of HCN1 channels in the binaural auditory brainstem of the naked mole-rat (Heterocephalus glaber). PLoS One 11:e0146428

    Google Scholar 

  • Gómez-Álvarez M, Gourévitch B, Felix RA, Nyberg T, Hernández-Montiel HL, Magnusson AK (2018) Temporal information in tones, broadband noise, and natural vocalizations is conveyed by differential spiking responses in the superior paraolivary nucleus. Eur J Neurosci 48:2030–2049

    Article  PubMed  Google Scholar 

  • Groff JA, Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90:3178–3200

    Article  PubMed  Google Scholar 

  • Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012

    Article  CAS  PubMed  Google Scholar 

  • Guinan JJ Jr (2018) Olivocochlear efferents: their action, effects, measurement and uses, and the impact of the new conception of cochlear mechanical responses. Hear Res 362:38–47

    Article  PubMed  Google Scholar 

  • Gultekin YB, Hage SR (2018) Limiting parental interaction during vocal development affects acoustic call structure in marmoset monkeys. Sci Adv 4:eaar4012

    Article  PubMed  PubMed Central  Google Scholar 

  • Hadland KA, Rushworth MFS, Gaffan D, Passingham RE (2003) The effect of cingulate lesions on social behaviour and emotion. Neuropsychologia 41:919–931

    Article  CAS  PubMed  Google Scholar 

  • Heffner HE, Heffner RS, Contos C, Ott T (1994) Audiogram of the hooded Norway rat. Hear Res 73:244–247

    Article  CAS  PubMed  Google Scholar 

  • Heffner HE, Masterton B (1980) Hearing in glires: domestic rabbit, cotton rat, feral house mouse, and kangaroo rat. J Acoust Soc Am 68:1584–1599

    Article  Google Scholar 

  • Heffner RS, Heffner HE (1990) Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear Res 46:239–252

    Google Scholar 

  • Heffner RS, Heffner HE (1992) Hearing and sound localization in blind mole rats (Spalax ehrenbergi). Hear Res 62:206–216

    Google Scholar 

  • Heffner RS, Heffner HE (1993) Degenerate hearing and sound localization in naked mole rats (Heterocephalus glaber), with an overview of central auditory structures. J Comp Neurol 331:418–433

    Google Scholar 

  • Heth G, Frankenberg E, Nevo E (1986) Adaptive optimal sound for vocal communication in tunnels of a subterranean mammal (Spalax ehrenbergi). Experientia 42:1287–1289

    Google Scholar 

  • Hill WCO, Porter A, Bloom RT, Seago J, Southwick MD (1957) Field and laboratory studies on the naked mole rat, Heterocephalus glaber. Proc Zool Soc Lond 128:455–514

    Google Scholar 

  • Holekamp KE, Sakai ST, Lundrigan BL (2007) Social intelligence in the spotted hyena (Crocuta crocuta). Philos Trans R Soc Lond Ser B Biol Sci 362:523–538

    Google Scholar 

  • Holmes MM, Goldman BD (2021) Social behavior in naked mole-rats: individual differences in phenotype and proximate mechanisms of mammalian eusociality. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 35–58

    Google Scholar 

  • Hossain WA, Antic SD, Yang Y, Rasband MN, Morest DK (2005) Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J Neurosci 25:6857–6868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irving S, Moore DR, Liberman MC, Sumner CJ (2011) Olivocochlear efferent control in sound localization and experience-dependent learning. J Neurosci 31:2493–2501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito T, Bishop DC, Oliver DL (2011) Expression of glutamate and inhibitory amino acid vesicular transporters in the rodent auditory brainstem. J Comp Neurol 519:316–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarvis ED (2019) Evolution of vocal learning and spoken language. Science 366:50–54

    Article  CAS  PubMed  Google Scholar 

  • Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573

    Article  CAS  PubMed  Google Scholar 

  • Jarvis JUM (1991) Chapter 13: Reproduction of naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 384–425

    Google Scholar 

  • Kapfer C, Seidl AH, Schweizer H, Grothe B (2002) Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci 5:247–253

    Article  CAS  PubMed  Google Scholar 

  • Khurana S, Remme MWH, Rinzel J, Golding NL (2011) Dynamic interaction of Ih and IK-LVA during trains of synaptic potentials in principal neurons of the medial superior olive. J Neurosci 31:8936–8947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YH, Holt JR (2013) Functional contributions of HCN channels in the primary auditory neurons of the mouse inner ear. J Gen Physiol 142:207–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King SL, Friedman WR, Allen SJ, Gerber L, Jensen FH, Wittwer S, Connor RC, Krützen M (2018) Bottlenose dolphins retain individual vocal labels in multi-level alliances. Curr Biol CB 28:1993–1999.e3

    Article  CAS  PubMed  Google Scholar 

  • King SL, Janik VM (2013) Bottlenose dolphins can use learned vocal labels to address each other. Proc Natl Acad Sci U S A 110:13216–13221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirzinger A, Jürgens U (1982) Cortical lesion effects and vocalization in the squirrel monkey. Brain Res 233:299–315

    Article  CAS  PubMed  Google Scholar 

  • Knörnschild M, Fernandez AA, Nagy M (2019) Vocal information and the navigation of social decisions in bats: is social complexity linked to vocal complexity? Fox C, ed. Funct Ecol 34:322–331

    Article  Google Scholar 

  • Koch U, Braun M, Kapfer C, Grothe B (2004) Distribution of HCN1 and HCN2 in rat auditory brainstem nuclei. Eur J Neurosci 20:79–91

    Article  PubMed  Google Scholar 

  • Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rübsamen R (2003) Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23:9199–9207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kössl M, Frank G, Burda H, Muller M (1996) Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec. J Comp Physiol A 178:427–434

    Google Scholar 

  • Lacey EA, Alexander RD, Braude SH, Sherman PW, Jarvis JUM (1991) An ethogram for the naked mole-rat: nonvocal behaviors. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 209–242

    Google Scholar 

  • Lange S, Burda H, Wegner RE, Dammann P, Begall S, Kawalika M (2007) Living in a “stethoscope”: burrow-acoustics promote auditory specializations in subterranean rodents. Naturwissenschaften 94:134–138

    Article  CAS  PubMed  Google Scholar 

  • Larson J, Park TJ (2009) Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20:1634–1637

    Article  PubMed  Google Scholar 

  • Leao RN, Svahn K, Berntson A, Walmsley B (2005) Hyperpolarization-activated (Ih) currents in auditory brainstem neurons of normal and congenitally deaf mice. Eur J Neurosci 22:147–157

    Article  PubMed  Google Scholar 

  • Lesica NA, Lingner A, Grothe B (2010) Population coding of interaural time differences in gerbils and barn owls. J Neurosci 30:11696–11702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lesicko AMH, Hristova TS, Maigler KC, Llano DA (2016) Connectional modularity of top- down and bottom-up multimodal inputs to the lateral cortex of the mouse inferior colliculus. J Neurosci 36:11037–11050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewin GR, Smith ESJ, Reznick J, Debus K, Barker A, Park TJ (2021) The somatosensory world of the African naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 197–220

    Google Scholar 

  • Lindzey G, Winston H, Manosevitz M (1961) Social dominance in inbred mouse strains. Nature 191:474–476

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Poveda EA (2018) Olivocochlear efferents in animals and humans: from anatomy to clinical relevance. Front Neurol 9:197

    Article  PubMed  PubMed Central  Google Scholar 

  • MacLean PD, Newman JD (1988) Role of midline frontolimbic cortex in production of the isolation call of squirrel monkeys. Brain Res 450:111–123

    Article  CAS  PubMed  Google Scholar 

  • Mason MJ, Cornwall HL, Smith ESJ (2016) Ear structures of the naked mole-rat, Heterocephalus glaber, and its relatives (Rodentia: Bathyergidae). PLoS One 11:e0167079

    Google Scholar 

  • Mason MJ, Lai FW, Li JG, Nevo E (2010) Middle ear structure and bone conduction in Spalax, Eospalax, and Tachyoryctes mole-rats (Rodentia: Spalacidae). J Morphol 271:462–472

    PubMed  Google Scholar 

  • Mathevon N, Koralek A, Weldele M, Glickman SE, Theunissen FE (2010) What the hyena’s laugh tells: sex, age, dominance and individual signature in the giggling call of Crocuta crocuta. BMC Ecol 10:9

    Article  PubMed  PubMed Central  Google Scholar 

  • May-Collado LJ, Agnarsson I, Wartzok D (2007) Phylogenetic review of tonal sound production in whales in relation to sociality. BMC Evol Biol 7:136

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller M (1996) The cochlear place-frequency map of the adult and developing Mongolian gerbil. Hear Res 94:148–156

    Article  PubMed  Google Scholar 

  • Müller M, Burda H (1989) Restricted hearing range in a subterranean rodent, Cryptomys hottentotus. Naturwissenschaften 76:134–135

    Google Scholar 

  • O’Connor TP, Lee A, Jarvis JU, Buffenstein R (2002) Prolonged longevity in naked mole-rats: age-related changes in metabolism, body composition and gastrointestinal function. Comp Biochem Physiol Mol Integr Physiol 133:835–842

    Article  Google Scholar 

  • Oertel D (1997) Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19:959–962

    Article  CAS  PubMed  Google Scholar 

  • Okanoya K, Yosida S, Barone CM, Applegate DT, Brittan-Powell EF, Dooling RJ, Park TJ (2018) Auditory-vocal coupling in the naked mole-rat, a mammal with poor auditory thresholds. J Comp Physiol A 204:905–914

    Article  Google Scholar 

  • Oliver DL, Cant NB (2018) Introduction to mammalian auditory pathways. In: Oliver DL, Cant NB, Fay RR, Popper AN (eds) The Mammalian Auditory Pathways: Synaptic Organization and Microcircuits. Springer, Cham, pp 1–6

    Google Scholar 

  • Ordóñez-Gómez JD, Santillan-Doherty AM, Hammerschmidt K (2019) Acoustic variation of spider monkey (Ateles geoffroyi) contact calls is related to caller isolation and affects listeners’ responses. PLoS One 14:e0213914

    Google Scholar 

  • Park TJ, Comer C, Carol A, Lu Y, Hong HS, Rice FL (2003) Somatosensory organization and behavior in naked mole-rats: II. Peripheral structures, innervation, and selective lack of neuropeptides associated with thermoregulation and pain. J Comp Neurol 465(1):104–120

    Google Scholar 

  • Park TJ, Smith ESJ, Reznick J, Bennett NC, Applegate DT, Larson J, Lewin GR (2021) African naked mole-rats demonstrate extreme tolerance to hypoxia and hypercapnia. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 255-269

    Google Scholar 

  • Park TJ et al (2017) Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat. Science 356:307–311

    Article  CAS  PubMed  Google Scholar 

  • Penz OK, Fuzik J, Kurek AB, Romanov R, Larson J, Park TJ, Harkany T, Keimpema E (2015) Protracted brain development in a rodent model of extreme longevity. Sci Rep 5:11592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pepper JW, Braude SH, Lacey EA, Sherman PW (1991) Vocalizations of the naked mole-rat. In: The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 243–274

    Google Scholar 

  • Pollard KA, Blumstein DT (2012) Evolving communicative complexity: insights from rodents and beyond. Philos Trans R Soc B Biol Sci 367:1869–1878

    Article  Google Scholar 

  • Pomberger T, Risueno-Segovia C, Löschner J, Hage SR (2018) Precise motor control enables rapid flexibility in vocal behavior of marmoset monkeys. Curr Biol 28:788–794.e3

    Article  CAS  PubMed  Google Scholar 

  • Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci JAALAS 46:28–34

    CAS  PubMed  Google Scholar 

  • Prat Y, Taub M, Yovel Y (2016) Everyday bat vocalizations contain information about emitter, addressee, context, and behavior. Sci Rep 6:39419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyott SJ, Duncan RK (2016) BK channels in the vertebrate inner ear. Int Rev Neurobiol 128:369–399

    Article  CAS  PubMed  Google Scholar 

  • Pyott SJ, van Tuinen M, Screven LA, Schrode KM, Bai J-P, Barone, CM, Price, SD, Lysakowski A, Sanderford M, Kumar S, Santos-Sacchi J, Lauer AM, Park TJ (2020) Functional, morphological, and evolutionary characterization of hearing in subterranean, eusocial African mole-rats. Curr Biol 30(22):4329–4341

    Google Scholar 

  • Quilliam TA (1966) The mole’s sensory apparatus. J Zool 149

    Google Scholar 

  • Raphael Y, Lenoir M, Wroblewski R, Pujol R (1991) The sensory epithelium and its innervation in the mole rat cochlea. J Comp Neurol 314:367–382

    Article  CAS  PubMed  Google Scholar 

  • Reeve HK (1992) Queen activation of lazy workers in colonies of the eusocial naked mole-rat. Nature 358:147–149

    Article  CAS  PubMed  Google Scholar 

  • Reijntjes DOJ, Pyott SJ (2016) The afferent signaling complex: regulation of type I spiral ganglion neuron responses in the auditory periphery. Hear Res 336:1–16

    Article  PubMed  Google Scholar 

  • Reznick J, Park TJ, Lewin GR (2021) A sweet story of metabolic innovation in the naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 271–286

    Google Scholar 

  • Ruby JG, Smith M, Buffenstein R (2018) Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age. eLife 7:e31157

    Google Scholar 

  • Ryan A (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59:1222–1226

    Google Scholar 

  • Sahd L, Bennett NC, Kotzé SH (2019) Hind foot drumming: morphological adaptations of the muscles and bones of the hind limb in three African mole-rat species. J Anat 235:811–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 33:13686–13694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmons DD (2002) Development of the inner ear efferent system across vertebrate species. J Neurobiol 53:228–250

    Article  PubMed  Google Scholar 

  • Skulachev VP, Holtze S, Vyssokikh MY, Bakeeva LE, Skulachev MV, Markov AV, Hildebrandt TB, Sadovnichii VA (2017) Neoteny, prolongation of youth: from naked mole rats to “naked apes” (humans). Physiol Rev 97:699–720

    Article  PubMed  Google Scholar 

  • Snowdon CT, Hausberger M (eds) (1997) Social Influences on Vocal Development, 1st edn. Cambridge University Press

    Google Scholar 

  • Spoendlin H (1972) Innervation densities of the cochlea. Acta Otolaryngol 73:235–248

    Article  CAS  PubMed  Google Scholar 

  • Trattner B, Gravot CM, Grothe B, Kunz L (2013) Metabolic maturation of auditory neurones in the superior olivary complex. PLoS One 8:e67351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanden Hole C, Van Daele PAAG, Desmet N, Devos P, Adriaens D (2014) Does sociality imply a complex vocal communication system? A case study for Fukomys micklemi (Bathyergidae, Rodentia). Bioacoustics 23:143–160

    Google Scholar 

  • Vice EN, Lagestee S, Browe BM, Deb D, Smith ESJ, Park TJ (2021) Sensory systems of the African naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 137–156

    Google Scholar 

  • Vrettakos PA, Dear SP, Saunders JC (1988) Middle ear structure in the chinchilla: a quantitative study. Am J Otolaryngol 9:58–67

    Article  CAS  PubMed  Google Scholar 

  • Wangemann P (2006) Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 576:11–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weitekamp CA, Hofmann HA (2014) Evolutionary themes in the neurobiology of social cognition. Curr Opin Neurobiol 28:22–27

    Article  CAS  PubMed  Google Scholar 

  • Yahav S, Buffenstein R (1992) Caecal function provides the energy of fermentation without liberating heat in the poikilothermic mammal, Heterocephalus glaber. J Comp Physiol B 162(3):216–218

    Google Scholar 

  • Yi E, Roux I, Glowatzki E (2010) Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103:2532–2543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yosida S, Kobayasi KI, Ikebuchi M, Ozaki R, Okanoya K (2007) Antiphonal vocalization of a subterranean rodent, the naked mole-rat (Heterocephalus glaber). Ethology 113:703–710

    Google Scholar 

  • Yosida S, Okanoya K (2009) Naked mole-rat is sensitive to social hierarchy encoded in antiphonal vocalization. Ethology 115:823–831

    Article  Google Scholar 

  • Yosida S, Okanoya K (2012) Bilateral lesions of the medial frontal cortex disrupt recognition of social hierarchy during antiphonal communication in naked mole-rats (Heterocephalus glaber). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 198:109–117

    Google Scholar 

  • Yovel Y, Melcon ML, Franz MO, Denzinger A, Schnitzler H-U (2009) The voice of bats: how greater mouse-eared bats recognize individuals based on their echolocation calls Friston KJ, ed. PLoS Comput Biol 5:e1000400

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu WM, Goodrich LV (2014) Morphological and physiological development of auditory synapses. Hear Res 311:3–16

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The work in the authors‘ laboratories has been supported by the following agencies: the University of Groningen (the Netherlands) and the Heinsius-Houbolt Foundation to SJP and ERC advanced grants to GRL (AdG 789128 and AdG 294678).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sonja J. Pyott .

Editor information

Editors and Affiliations

Glossary

Fundamental frequency

lowest frequency of a periodic waveform. This is usually the lowest frequency in a harmonic sound.

Hyperpolarization-activated cyclic nucleotide gated (HCN) 1 channels

HCN channels are a family of voltage-gated ion channels that open upon hyperpolarization and are modulated by cAMP inside the neuron. They are permeable for Na+-ions and to a lesser extent to K+-ion and are thus depolarizing and can induce pacemaker activity. Among the four isoforms the HCN1 channels are t activated at the most depolarized voltage (around -45 mV) and have the fastest activation time constants.

Kv1 channels

Kv1 channels are a family of voltage-gated ion channels that are permeable for K+-ions and thus hyperpolarizing. Compared to other voltage-gated K+-channels they are activated at more hyperpolarized voltages, closer to the membrane resting potential.

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Barker, A.J., Koch, U., Lewin, G.R., Pyott, S.J. (2021). Hearing and Vocalizations in the Naked Mole-Rat. In: Buffenstein, R., Park, T.J., Holmes, M.M. (eds) The Extraordinary Biology of the Naked Mole-Rat. Advances in Experimental Medicine and Biology, vol 1319. Springer, Cham. https://doi.org/10.1007/978-3-030-65943-1_6

Download citation

Publish with us

Policies and ethics