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Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice
Abstract
Multiple-unit threshold curves (MTCs) were obtained from inferior colliculus (IC) neurons across much of the (approximately 2-2.5 yr) life-span of two inbred mouse strains: the C57BL/6, which undergoes progressive age-related sensorineural hearing loss; and the CBA, which maintains good sensitivity until well into the second year of life. Tonotopic organization (the orderly dorsoventral arrangement of frequency sensitivity) is disrupted in the IC central nucleus (ICC) of aging C57 mice. Dorsal (low-frequency) MTCs change little during the first year of life, but in more ventral (high-frequency) regions high-frequency portions of MTCs are eliminated, best frequencies become lower, and low-frequency thresholds are reduced. These changes make the curves more similar to one another along the dorsoventral axis. During the second year of life, all thresholds become greatly elevated with neurons throughout the IC responding only to middle frequencies at very high intensities. In C57 mice, Q10 ratios (a measure of MTC tip sharpness) decline after 7 mo. The decline of Q10 with aging is associated with the age-related lowering of best frequencies and elevation of thresholds, both of which are positively correlated with smaller Q10s. The frequency range of C57 MTCs begins to decrease at 14 mo of age, when hearing loss is quite severe at all frequencies. In CBA mice, the above changes are minimal or do not occur even in 22 mo olds, which have moderate loss of sensitivity across all frequencies. Even in young mice (prior to demonstrable cochlear pathology in C57 mice), there are differences in MTCs between the two strains employed, with sensitivity of CBA mice being "shifted" toward higher frequencies. Age-related changes in MTC properties depend on the pattern of hearing loss (e.g., high frequency vs. flat) and the dorsoventral location of neurons within the ICC.
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“As there is a well-characterized loss of hearing around 7 months of age in the C57BL/6J strain [46–50]”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [48]
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“Ultra- at high frequencies and progress with age (Willott, 1986; Q. Y. Zheng et al., 1999; White et al., 2000; Lang et al., 2002).”
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“A similar frequency reorganization in the IC of C57 mice has been reported (Willott, 1986).”
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“Willott (1986) described changes in the ICC of C57BL/6J (C57) mice, a strain that suffers a form of sensorineural pathology that results in high-frequency hearing losses in early adulthood.”
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“Previous studies have demonstrated that C57BL/6 J mice display early onset of age-related hearing loss [22-24].”
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“…to neurons in middle-frequency regions, and more relatively simple acoustico-motor behavior, the ASR is ame- vigorous suprathreshold responses are evoked by middlenable to neurobehavioral research on human and nonhuman frequency tones (Willott 1984, 1986; Willott et al. 1988, subjects (Davis 1984).”
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Anatomic and physiologic aging: a behavioral neuroscience perspective.
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“When compared with their own performance at one month of age, C57BL/6J mice also show a mild high frequency hearing loss by two months of age, which becomes more pronounced by six or seven months (Willott 1986; Li and Borg 1991).”
Willott, J. F., & Bross, L. S. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(95)00188-3 · Cited by 63
Self-citationMeasurement of the Auditory Brainstem Response (ABR) to Study Auditory Sensitivity in Mice
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Self-citationKazee, A. M., Han, L. Y., Spongr, V. P., Walton, J. P., Salvi, R., & Flood, D. G. (1995) · Hearing Research · doi:10.1016/0378-5955(95)00128-6 · Cited by 61
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Morphology of the dorsal cochlear nucleus in C57BL/6J and CBA/J mice across the life span
Willott, J. F., Bross, L. S., & McFadden, S. L. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210412 · Cited by 61
Self-citationDopamine Modulates Auditory Responses in the Inferior Colliculus in a Heterogeneous Manner
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“Willott (1986) showed a similar trend for inferior colliculus tuning curve thresholds with most of the change seen by 14 months.”
Beckmann, D., Feldmann, M., Shchyglo, O., & Manahan‐Vaughan, D. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa061 · Cited by 54
Age-Related Changes in Cochlear Endolymphatic Potassium and Potential in CD-1 and CBA/CaJ Mice
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“AHL in the CD-1 strain has not been studied as extensively as in C57BL/6, although both mouse strains are known to have early sensorineural hearing loss that is probably genetically determined (Le Calvez et al. 1998a, Shone et al. 1991; Walton et al. 1995; Willott 1986).”
BackgroundGould, T. J., & Feiro, O. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.040 · Cited by 56
Johnson, K. R., Yu, H., Ding, D., et al. (2010) · Hearing Research · doi:10.1016/j.heares.2010.05.002 · Cited by 56
“Age-related hearing loss (AHL) or presbycusis is a major health concern because of its widespread occurrence among the elderly and its negative influence on their quality of life (Dalton et al., 2003).”
InfluentialGourévitch, B., & Edeline, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07905.x · Cited by 53
“…in aged C57 mice have emphasized an age-related elevation of thresholds mostly in the ventral cochlear nucleus (Willott et al., 1991), whereas the thresholds were similar or moderately affected in the dorsal cochlear nucleus, IC and AI (Willott, 1986, 1991; Willott et al., 1988, 1991, 1993).”
BackgroundWalton, J. P., Barsz, K., & Wilson, W. W. (2007) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s10162-007-0101-z · Cited by 50
“Along with extensive reorganization of the tonotopic map of the IC (Willott 1986, Irvine et al. 2003, Wang et al. 1996), Barsz et al. (2007) reported that IC units from hearing-impaired mice displayed broader frequency receptive fields.”
BackgroundMethodSpatial organization of receptive fields in the auditory midbrain of awake mouse
Portfors, C. V., Mayko, Z. M., Jonson, K., et al. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.025 · Cited by 50
“…F. CHA,a AND P. D. ROBERTS,b aSchool of Biological Sciences, Washington State University, 14204 E Salmon Creek Ave., Vancouver, WA 98686, USA bDivision of Biomedical Engineering, Oregon Health and Science Uniersity, 3181 S.W. Jackson Park Rd., Portland, OR 97239, USA Abstract—Efficient encoding…”
BackgroundWillott, J. F., & Bross, L. S. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20065 · Cited by 48
“The frequency range of hearing in young B6 mice is 2kHz to 64 kHz (Willott, 1986), whereas the bandwidth of the AAE noise encompasses relative middle frequencies, with little energy below 4 kHz or above 32 kHz.”
BackgroundSelf-citationPharmacology of the Inferior Colliculus
Kelly, J. B., & Caspary, D. M. (2005) · Springer eBooks · doi:10.1007/0-387-27083-3_9 · Cited by 49
Hereditary deafness occurring in cd/1 mice
Shone, G., Raphael, Y., & Miller, J. M. (1991) · Hearing Research · doi:10.1016/0378-5955(91)90084-m · Cited by 48
Willott, J. F., & Carlson, S. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.3.396 · Cited by 53
Self-citationOver-expression of X-linked inhibitor of apoptosis protein slows presbycusis in C57BL/6J mice
Wang, J., Menchenton, T., Yin, S., Yu, Z., Bance, M., Morris, D. P., Moore, C. S., Korneluk, R. G., & Robertson, G. S. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.07.016 · Cited by 47
Willott, J. F., Turner, J. G., & Sundin, V. (2000) · Hearing Research · doi:10.1016/s0378-5955(00)00014-9 · Cited by 47
Self-citationInhibition shapes selectivity to vocalizations in the inferior colliculus of awake mice
Mayko, Z. M., Roberts, P. D., & Portfors, C. V. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00073 · Cited by 46
“The CBA/CaJ strain exhibits normal hearing sensitivity into its second year of life (Willott, 1986, 1991, 2005).”
BackgroundMultivariate search for differentially expressed gene combinations
Xiao, Y., Frisina, R. D., Gordon, A. Y., Klebanov, L. B., & Yakovlev, A. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-164 · Cited by 45
“, vestibulocochlear) fibers, and develop stria vascularis/potassium recycling metabolic problems that degrade audibility and spectral tuning [17-21].”
BackgroundA comparison of the behavior of C57BL/6 and C57BL/10 mice
Deacon, R. M. J., Thomas, C., Rawlins, J. N. P., et al. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.009 · Cited by 46
O’Neill, W. W., Zettel, M. L., Whittemore, K. R., & Frisina, R. D. (1997) · Hearing Research · doi:10.1016/s0378-5955(97)00116-0 · Cited by 46
Endocochlear potentials and compound action potential recovery: functions in the C57BL/6J mouse
Lang, H., Schulte, B. A., & Schmiedt, R. A. (2002) · Hearing Research · doi:10.1016/s0378-5955(02)00552-x · Cited by 46
ERK2 mediates inner hair cell survival and decreases susceptibility to noise-induced hearing loss
Kurioka, T., Matsunobu, T., Satoh, Y., Niwa, K., Endo, S., Fujioka, M., & Shiotani, A. (2015) · Scientific Reports · doi:10.1038/srep16839 · Cited by 44
Morphology of the inferior colliculus in C57BL/6J and CBA/J mice across the life span
Willott, J. F., Bross, L. S., & McFadden, S. L. (1994) · Neurobiology of Aging · doi:10.1016/0197-4580(94)90109-0 · Cited by 45
Self-citationMuniak, M. A., Ayeni, F. E., & Ryugo, D. K. (2018) · Hearing Research · doi:10.1016/j.heares.2018.03.021 · Cited by 43
“…the CBA genotype has been widely accepted as representing normal hearing, and its auditory functions have routinely been compared with those of mice with various forms of hereditary hearing loss (e.g., Connelly et al., 2017; Limb and Ryugo, 2000; Willott, 1984, 1986; Willott et al., 1991).”
BackgroundWillott, J. F., & Turner, J. G. (2000) · Hearing Research · doi:10.1016/s0378-5955(00)00137-4 · Cited by 43
Self-citationLow-Frequency Tone Pips Elicit Exaggerated Startle Reflexes in C57BL/6J Mice with Hearing Loss
Ison, J. R., & Allen, P. D. (2003) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s10162-002-3046-2 · Cited by 42
“Their increased sensitivity is seen most strongly in auditory cortex (Willott et al. 1993), but is present also throughout the central nucleus of the inferior colliculus (Willott 1986) and, to a lesser extent, in the dorsal cochlear nucleus (Willott et al. 1991).”
BackgroundWillott, J. F., Bross, L. S., & McFadden, S. L. (1994) · Hearing Research · doi:10.1016/0378-5955(94)90171-6 · Cited by 42
“Willott et al. / Hearing Research 74 (1994) 1-21”
BackgroundSelf-citationAdvantages of a Mouse Model for Human Hearing Impairment
Kikkawa, Y., Seki, Y., Okumura, K., et al. (2012) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.61.85 · Cited by 41
Metadata
- Authors
- Willott, J. F.
- Corresponding author
- Willott, J. F.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1986-08-01
- Volume
- 56
- Issue
- 2
- Pages
- 391-408
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1921685703
- Cited by
- 211
- References
- 0
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 5 · 2023: 6 · 2022: 4 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 3 · 2016: 7 · 2015: 3 · 2014: 5 · 2013: 13 · 2012: 7
- FWCI
- 1.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k04ag000234-05)
- National Institute on Aging (KO4-AG-00234, R01-AG-03069)
- National Center for Research Resources (RR07176)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Health Sciences › Health Professions › Speech and Hearing › Hearing Loss and Rehabilitation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- inferior colliculus, age-related hearing loss, sensorineural hearing loss, tonotopic organization, characteristic frequency, Q10, central nucleus of inferior colliculus, anatomical location, C57BL/6 mice, CBA mice, mouse strain differences, auditory sensitivity, auditory brainstem
- MeSH terms
- Acoustic Stimulation, Aging, Animals, Auditory Pathways, Hearing Loss, Sensorineural, Inferior Colliculi, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Mice, Inbred Strains, Neurons, Afferent, Sensory Thresholds, Species Specificity, Mice
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