Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice

Willott, J. F.

doi:10.1152/jn.1986.56.2.391

Cited by 211Hearing, Cochlea, Tinnitus, GeneticsHearing Loss and RehabilitationNeuroscience and Music Perception

Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice

Willott, J. F.·1986·Journal of Neurophysiology

DOI 10.1152/jn.1986.56.2.391

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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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There is a well-characterized loss of hearing around 7 months of age in the C57BL/6J strain.
“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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“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).”
Morphological changes in the anteroventral cochlear nucleus that accompany sensorineural hearing loss in DBA/2J and C57BL/6J mice
Willott, J. F., & Bross, L. S. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(95)00188-3 · Cited by 63 · see citing works
Self-citation
Measurement of the Auditory Brainstem Response (ABR) to Study Auditory Sensitivity in Mice
Willott, J. F. (2006) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0821bs34 · Cited by 62 · see citing works
Self-citation
Synaptic loss in the central nucleus of the inferior colliculus correlates with sensorineural hearing loss in the C57BL/6 mouse model of presbycusis
Kazee, 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 · see citing works
Sex- and age-related elevation of cochlear nerve envelope response (CNER) and auditory brainstem response (ABR) thresholds in C57BL/6 mice
Henry, K. R. (2002) · Hearing Research · doi:10.1016/s0378-5955(02)00391-x · Cited by 61 · see citing works
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 · see citing works
Self-citation
Dopamine Modulates Auditory Responses in the Inferior Colliculus in a Heterogeneous Manner
Gittelman, J. X., Perkel, D. J., & Portfors, C. V. (2013) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s10162-013-0405-0 · Cited by 57 · see citing works
Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice
Brewton, D. H., Kokash, J., Jimenez, O., Pena, E. R., & Razak, K. A. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00270 · Cited by 54 · see citing works
“Willott (1986) showed a similar trend for inferior colliculus tuning curve thresholds with most of the change seen by 14 months.”
Hippocampal Synaptic Plasticity, Spatial Memory, and Neurotransmitter Receptor Expression Are Profoundly Altered by Gradual Loss of Hearing Ability
Beckmann, D., Feldmann, M., Shchyglo, O., & Manahan‐Vaughan, D. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa061 · Cited by 52 · see citing works
Age-Related Changes in Cochlear Endolymphatic Potassium and Potential in CD-1 and CBA/CaJ Mice
Wu, T., & Marcus, D. C. (2003) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s10162-002-3026-6 · Cited by 58 · see citing works
“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).”
Background
Age-related deficits in the retention of memories for cued fear conditioning are reversed by galantamine treatment
Gould, T. J., & Feiro, O. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.040 · Cited by 56 · see citing works
Separate and combined effects of Sod1 and Cdh23 mutations on age-related hearing loss and cochlear pathology in C57BL/6J mice
Johnson, K. R., Yu, H., Ding, D., et al. (2010) · Hearing Research · doi:10.1016/j.heares.2010.05.002 · Cited by 56 · see citing works
“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).”
Influential
Age‐related changes in the guinea pig auditory cortex: relationship with brainstem changes and comparison with tone‐induced hearing loss
Gourévitch, B., & Edeline, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07905.x · Cited by 53 · see citing works
“…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).”
Background
Sensorineural Hearing Loss and Neural Correlates of Temporal Acuity in the Inferior Colliculus of the C57bl/6 Mouse
Walton, 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 · see citing works
“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.”
BackgroundMethod
Spatial 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 · see citing works
“…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…”
Background
Effects of prolonged exposure to an augmented acoustic environment on the auditory system of middle‐aged C57BL/6J mice: Cochlear and central histology and sex differences
Willott, J. F., & Bross, L. S. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20065 · Cited by 48 · see citing works
“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-citation
Pharmacology of the Inferior Colliculus
Kelly, J. B., & Caspary, D. M. (2005) · Springer eBooks · doi:10.1007/0-387-27083-3_9 · Cited by 49 · see citing works
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 · see citing works
Modification of the acoustic startle response in hearing-impaired C57BL/6J mice: Prepulse augmentation and prolongation of prepulse inhibition.
Willott, J. F., & Carlson, S. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.3.396 · Cited by 48 · see citing works
Self-citation
Over-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 · see citing works
Effects of exposure to an augmented acoustic environment on auditory function in mice: roles of hearing loss and age during treatment
Willott, J. F., Turner, J. G., & Sundin, V. (2000) · Hearing Research · doi:10.1016/s0378-5955(00)00014-9 · Cited by 47 · see citing works
Self-citation
Inhibition 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 · see citing works
“The CBA/CaJ strain exhibits normal hearing sensitivity into its second year of life (Willott, 1986, 1991, 2005).”
Background
Multivariate 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 · see citing works
“, vestibulocochlear) fibers, and develop stria vascularis/potassium recycling metabolic problems that degrade audibility and spectral tuning [17-21].”
Background
A 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 · see citing works
Calbindin D-28k immunoreactivity in the medial nucleus of the trapezoid body declines with age in C57BL/6, but not CBA/CaJ, mice
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citation
Hidden hearing loss and endbulbs of Held: Evidence for central pathology before detection of ABR threshold increases
Muniak, M. A., Ayeni, F. E., & Ryugo, D. K. (2018) · Hearing Research · doi:10.1016/j.heares.2018.03.021 · Cited by 44 · see citing works
“…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).”
Background
Neural plasticity in the mouse inferior colliculus: relationship to hearing loss, augmented acoustic stimulation, and prepulse inhibition
Willott, J. F., & Turner, J. G. (2000) · Hearing Research · doi:10.1016/s0378-5955(00)00137-4 · Cited by 43 · see citing works
Self-citation
Low-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 · see citing works
“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).”
Background
Morphology of the cochlear nucleus in CBA/J mice with chronic, severe sensorineural cochlear pathology induced during adulthood
Willott, J. F., Bross, L. S., & McFadden, S. L. (1994) · Hearing Research · doi:10.1016/0378-5955(94)90171-6 · Cited by 42 · see citing works
“Willott et al. / Hearing Research 74 (1994) 1-21”
BackgroundSelf-citation
Advantages 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 · see citing works

Observations on Tonotopic Organization within the Rat Inferior Colliculus Using 2‐Deoxy‐D[1‐3H] Glucose
Coleman, J. R., Campbell, M., & Clerici, W. J. (1982) · Otolaryngology · doi:10.1177/019459988209000621 · Cited by 20 · see citing works
Time of origin of neurons of the rat inferior colliculus and the relations between cytogenesis and tonotopic order in the auditory pathway
Altman, J., & Bayer, S. A. (1981) · Experimental Brain Research · doi:10.1007/bf00237506 · Cited by 84 · see citing works
Analysis of inferior colliculus in deaf chinchillas.
Shirane, M., Harada, Y., & Harrison, R. V. (1989) · Practica Oto-Rhino-Laryngologica · doi:10.5631/jibirin.82.1609
Plasticity of tonotopic maps in auditory midbrain following partial cochlear damage in the developing chinchilla
Harrison, R. V., Ibrahim, D., & Mount, R. J. (1998) · Experimental Brain Research · doi:10.1007/s002210050589 · Cited by 62 · see citing works
Spatial organization of frequency preference and selectivity in the human inferior colliculus
Martino, F. D., Moerel, M., de Moortele, P. V., Uǧurbil, K., Goebel, R., Yacoub, E. S., & Formisano, E. (2013) · Nature Communications · doi:10.1038/ncomms2379 · Cited by 114 · see citing works

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
DOI: 10.1152/jn.1986.56.2.391
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
Life Sciences › Neuroscience › Cognitive Neuroscience › 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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Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice

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