TY - JOUR
T1 - Altered response dynamics and increased population correlation to tonal stimuli embedded in noise in aging auditory cortex
AU - Shilling-Scrivo, Kelson
AU - Mittelstadt, Jonah
AU - Kanold, Patrick O.
N1 - Funding Information:
Received Apr. 18, 2021; revised Sep. 25, 2021; accepted Sep. 29, 2021. Author contributions: P.O.K. and K.S.-S. designed research; K.S.-S. and J.M. performed research; K.S.-S. and J.M. analyzed data; P.O.K. and K.S.-S. wrote the paper. This work was supported by the National Institute on Aging Grant P01 AG055365 (P.O.K.), the National Institutes of Health Grant RO1DC009607 (P.O.K.) and National Institutes of Health Grant T32DC000046 (K.S.-S.). We thank Nik Francis, Zac Bowen, Travis Babola, and Ji Liu for technical help. *K.S.-S. and J.M. contributed equally to this work. The authors declare no competing financial interests. Correspondence should be addressed to Patrick O. Kanold at pkanold@jhu.edu. https://doi.org/10.1523/JNEUROSCI.0839-21.2021 Copyright © 2021 the authors
Publisher Copyright:
Copyright © 2021 the authors.
PY - 2021/11/17
Y1 - 2021/11/17
N2 - Age-related hearing loss (presbycusis) is a chronic health condition that affects one-third of the world population. One hallmark of presbycusis is a difficulty hearing in noisy environments. Presbycusis can be separated into two components: alterations of peripheral mechanotransduction of sound in the cochlea and central alterations of auditory processing areas of the brain. Although the effects of the aging cochlea in hearing loss have been well studied, the role of the aging brain in hearing loss is less well understood. Therefore, to examine how age-related central processing changes affect hearing in noisy environments, we used a mouse model (Thy1-GCaMP6s X CBA) that has excellent peripheral hearing in old age. We used in vivo two-photon Ca21 imaging to measure the responses of neuronal populations in auditory cortex (ACtx) of adult (2–6months, nine male, six female, 4180 neurons) and aging mice (15–17months, six male, three female, 1055 neurons) while listening to tones in noisy backgrounds. We found that ACtx neurons in aging mice showed larger responses to tones and have less suppressed responses consistent with reduced inhibition. Aging neurons also showed less sensitivity to temporal changes. Population analysis showed that neurons in aging mice showed higher pairwise activity correlations and showed a reduced diversity in responses to sound stimuli. Using neural decoding techniques, we show a loss of information in neuronal populations in the aging brain. Thus, aging not only affects the responses of single neurons but also affects how these neurons jointly represent stimuli.
AB - Age-related hearing loss (presbycusis) is a chronic health condition that affects one-third of the world population. One hallmark of presbycusis is a difficulty hearing in noisy environments. Presbycusis can be separated into two components: alterations of peripheral mechanotransduction of sound in the cochlea and central alterations of auditory processing areas of the brain. Although the effects of the aging cochlea in hearing loss have been well studied, the role of the aging brain in hearing loss is less well understood. Therefore, to examine how age-related central processing changes affect hearing in noisy environments, we used a mouse model (Thy1-GCaMP6s X CBA) that has excellent peripheral hearing in old age. We used in vivo two-photon Ca21 imaging to measure the responses of neuronal populations in auditory cortex (ACtx) of adult (2–6months, nine male, six female, 4180 neurons) and aging mice (15–17months, six male, three female, 1055 neurons) while listening to tones in noisy backgrounds. We found that ACtx neurons in aging mice showed larger responses to tones and have less suppressed responses consistent with reduced inhibition. Aging neurons also showed less sensitivity to temporal changes. Population analysis showed that neurons in aging mice showed higher pairwise activity correlations and showed a reduced diversity in responses to sound stimuli. Using neural decoding techniques, we show a loss of information in neuronal populations in the aging brain. Thus, aging not only affects the responses of single neurons but also affects how these neurons jointly represent stimuli.
KW - Aging
KW - Auditory cortex
KW - Correlation
KW - Noise
KW - Offset
KW - Population
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U2 - 10.1523/JNEUROSCI.0839-21.2021
DO - 10.1523/JNEUROSCI.0839-21.2021
M3 - Article
C2 - 34611028
AN - SCOPUS:85120613592
SN - 0270-6474
VL - 34
SP - 9650
EP - 9668
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 3
ER -