Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation

Linda K McEvoy; Jaclyn Bergstrom; Donald J Hagler; David Wing; Emilie T Reas

doi:10.3233/JAD-230767

Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation

Linda K McEvoy, Jaclyn Bergstrom, Donald J Hagler, David Wing, Emilie T Reas

Faculty of Physical Education and Physical Therapy

Research output: Contribution to journal › Article › peer-review

Abstract

BACKGROUND: Hearing loss is associated with cognitive decline and increased risk for Alzheimer's disease, but the basis of this association is not understood.

OBJECTIVE: To determine whether hearing impairment is associated with advanced brain aging or altered microstructure in areas involved with auditory and cognitive processing.

METHODS: 130 participants, (mean 76.4±7.3 years; 65% women) of the Rancho Bernardo Study of Healthy Aging had a screening audiogram in 2003-2005 and brain magnetic resonance imaging in 2014-2016. Hearing ability was defined as the average pure tone threshold (PTA) at 500, 1000, 2000, and 4000 Hz in the better-hearing ear. Brain-predicted age difference (Brain-pad) was calculated as the difference between brain-predicted age based on a validated structural imaging biomarker of brain age, and chronological age. Regional diffusion metrics in temporal and frontal cortex regions were obtained from diffusion-weighted MRIs. Linear regression analyses adjusted for age, gender, education, and health-related measures.

RESULTS: PTAs were not associated with brain-PAD (β= 0.09; 95% CI: -0.084 to 0.243; p = 0.34). PTAs were associated with reduced restricted diffusion and increased free water diffusion primarily in right hemisphere temporal and frontal areas (restricted diffusion: βs = -0.21 to -0.30; 95% CIs from -0.48 to -0.02; ps < 0.03; free water: βs = 0.18 to 0.26; 95% CIs 0.01 to 0.438; ps < 0.04).

CONCLUSIONS: Hearing impairment is not associated with advanced brain aging but is associated with differences in brain regions involved with auditory processing and attentional control. It is thus possible that increased dementia risk associated with hearing impairment arises, in part, from compensatory brain changes that may decrease resilience.

Original language	English
Pages (from-to)	1163-1172
Number of pages	10
Journal	Journal of Alzheimer's Disease
Volume	96
Issue number	3
DOIs	https://doi.org/10.3233/JAD-230767
Publication status	Published - Nov 2023

Bibliographical note

Funding Information:
This work was supported by the National Institute on Aging (R00AG057797, R01AG077202 to ETR; R01AA021187 to LKM) and American Federation for Aging Research /McKnight Foundation (311122-00001 to ETR). Data collection for the Rancho Bernardo Study of Healthy Aging was provided primarily by the National Institutes of Health (including grant numbers: HV012160, AA021187, AG028507, AG007181, DK31801, HL034591, HS06726, and HL089622). Archiving and sharing of RBS data was supported by the National Institute on Aging: AG054067. RBS data is available through the RBS website: https://knit.ucsd.edu/ranchobernardostudy/

Publisher Copyright:
© 2023 – IOS Press. All rights reserved.

Keywords

Humans
Female
Male
Auditory Perception
Hearing
Brain/pathology
Hearing Loss
Water

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108324664Accepted author manuscript, 371 KBLicence: Unspecified

Cite this

@article{4230be2c491b43ba8d533a050134e18c,

title = "Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation",

abstract = "BACKGROUND: Hearing loss is associated with cognitive decline and increased risk for Alzheimer's disease, but the basis of this association is not understood.OBJECTIVE: To determine whether hearing impairment is associated with advanced brain aging or altered microstructure in areas involved with auditory and cognitive processing.METHODS: 130 participants, (mean 76.4±7.3 years; 65% women) of the Rancho Bernardo Study of Healthy Aging had a screening audiogram in 2003-2005 and brain magnetic resonance imaging in 2014-2016. Hearing ability was defined as the average pure tone threshold (PTA) at 500, 1000, 2000, and 4000 Hz in the better-hearing ear. Brain-predicted age difference (Brain-pad) was calculated as the difference between brain-predicted age based on a validated structural imaging biomarker of brain age, and chronological age. Regional diffusion metrics in temporal and frontal cortex regions were obtained from diffusion-weighted MRIs. Linear regression analyses adjusted for age, gender, education, and health-related measures.RESULTS: PTAs were not associated with brain-PAD (β= 0.09; 95% CI: -0.084 to 0.243; p = 0.34). PTAs were associated with reduced restricted diffusion and increased free water diffusion primarily in right hemisphere temporal and frontal areas (restricted diffusion: βs = -0.21 to -0.30; 95% CIs from -0.48 to -0.02; ps < 0.03; free water: βs = 0.18 to 0.26; 95% CIs 0.01 to 0.438; ps < 0.04).CONCLUSIONS: Hearing impairment is not associated with advanced brain aging but is associated with differences in brain regions involved with auditory processing and attentional control. It is thus possible that increased dementia risk associated with hearing impairment arises, in part, from compensatory brain changes that may decrease resilience.",

keywords = "Humans, Female, Male, Auditory Perception, Hearing, Brain/pathology, Hearing Loss, Water",

author = "McEvoy, {Linda K} and Jaclyn Bergstrom and Hagler, {Donald J} and David Wing and Reas, {Emilie T}",

note = "Funding Information: This work was supported by the National Institute on Aging (R00AG057797, R01AG077202 to ETR; R01AA021187 to LKM) and American Federation for Aging Research /McKnight Foundation (311122-00001 to ETR). Data collection for the Rancho Bernardo Study of Healthy Aging was provided primarily by the National Institutes of Health (including grant numbers: HV012160, AA021187, AG028507, AG007181, DK31801, HL034591, HS06726, and HL089622). Archiving and sharing of RBS data was supported by the National Institute on Aging: AG054067. RBS data is available through the RBS website: https://knit.ucsd.edu/ranchobernardostudy/ Publisher Copyright: {\textcopyright} 2023 – IOS Press. All rights reserved.",

year = "2023",

month = nov,

doi = "10.3233/JAD-230767",

language = "English",

volume = "96",

pages = "1163--1172",

journal = "Journal of Alzheimer's Disease",

issn = "1387-2877",

publisher = "IOS Press",

number = "3",

}

Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation. / McEvoy, Linda K; Bergstrom, Jaclyn; Hagler, Donald J; Wing, David; Reas, Emilie T.

In: Journal of Alzheimer's Disease, Vol. 96, No. 3, 11.2023, p. 1163-1172.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation

AU - McEvoy, Linda K

AU - Bergstrom, Jaclyn

AU - Hagler, Donald J

AU - Wing, David

AU - Reas, Emilie T

N1 - Funding Information: This work was supported by the National Institute on Aging (R00AG057797, R01AG077202 to ETR; R01AA021187 to LKM) and American Federation for Aging Research /McKnight Foundation (311122-00001 to ETR). Data collection for the Rancho Bernardo Study of Healthy Aging was provided primarily by the National Institutes of Health (including grant numbers: HV012160, AA021187, AG028507, AG007181, DK31801, HL034591, HS06726, and HL089622). Archiving and sharing of RBS data was supported by the National Institute on Aging: AG054067. RBS data is available through the RBS website: https://knit.ucsd.edu/ranchobernardostudy/ Publisher Copyright: © 2023 – IOS Press. All rights reserved.

PY - 2023/11

Y1 - 2023/11

N2 - BACKGROUND: Hearing loss is associated with cognitive decline and increased risk for Alzheimer's disease, but the basis of this association is not understood.OBJECTIVE: To determine whether hearing impairment is associated with advanced brain aging or altered microstructure in areas involved with auditory and cognitive processing.METHODS: 130 participants, (mean 76.4±7.3 years; 65% women) of the Rancho Bernardo Study of Healthy Aging had a screening audiogram in 2003-2005 and brain magnetic resonance imaging in 2014-2016. Hearing ability was defined as the average pure tone threshold (PTA) at 500, 1000, 2000, and 4000 Hz in the better-hearing ear. Brain-predicted age difference (Brain-pad) was calculated as the difference between brain-predicted age based on a validated structural imaging biomarker of brain age, and chronological age. Regional diffusion metrics in temporal and frontal cortex regions were obtained from diffusion-weighted MRIs. Linear regression analyses adjusted for age, gender, education, and health-related measures.RESULTS: PTAs were not associated with brain-PAD (β= 0.09; 95% CI: -0.084 to 0.243; p = 0.34). PTAs were associated with reduced restricted diffusion and increased free water diffusion primarily in right hemisphere temporal and frontal areas (restricted diffusion: βs = -0.21 to -0.30; 95% CIs from -0.48 to -0.02; ps < 0.03; free water: βs = 0.18 to 0.26; 95% CIs 0.01 to 0.438; ps < 0.04).CONCLUSIONS: Hearing impairment is not associated with advanced brain aging but is associated with differences in brain regions involved with auditory processing and attentional control. It is thus possible that increased dementia risk associated with hearing impairment arises, in part, from compensatory brain changes that may decrease resilience.

AB - BACKGROUND: Hearing loss is associated with cognitive decline and increased risk for Alzheimer's disease, but the basis of this association is not understood.OBJECTIVE: To determine whether hearing impairment is associated with advanced brain aging or altered microstructure in areas involved with auditory and cognitive processing.METHODS: 130 participants, (mean 76.4±7.3 years; 65% women) of the Rancho Bernardo Study of Healthy Aging had a screening audiogram in 2003-2005 and brain magnetic resonance imaging in 2014-2016. Hearing ability was defined as the average pure tone threshold (PTA) at 500, 1000, 2000, and 4000 Hz in the better-hearing ear. Brain-predicted age difference (Brain-pad) was calculated as the difference between brain-predicted age based on a validated structural imaging biomarker of brain age, and chronological age. Regional diffusion metrics in temporal and frontal cortex regions were obtained from diffusion-weighted MRIs. Linear regression analyses adjusted for age, gender, education, and health-related measures.RESULTS: PTAs were not associated with brain-PAD (β= 0.09; 95% CI: -0.084 to 0.243; p = 0.34). PTAs were associated with reduced restricted diffusion and increased free water diffusion primarily in right hemisphere temporal and frontal areas (restricted diffusion: βs = -0.21 to -0.30; 95% CIs from -0.48 to -0.02; ps < 0.03; free water: βs = 0.18 to 0.26; 95% CIs 0.01 to 0.438; ps < 0.04).CONCLUSIONS: Hearing impairment is not associated with advanced brain aging but is associated with differences in brain regions involved with auditory processing and attentional control. It is thus possible that increased dementia risk associated with hearing impairment arises, in part, from compensatory brain changes that may decrease resilience.

KW - Humans

KW - Female

KW - Male

KW - Auditory Perception

KW - Hearing

KW - Brain/pathology

KW - Hearing Loss

KW - Water

UR - http://www.scopus.com/inward/record.url?scp=85177983938&partnerID=8YFLogxK

U2 - 10.3233/JAD-230767

DO - 10.3233/JAD-230767

M3 - Article

C2 - 37955091

VL - 96

SP - 1163

EP - 1172

JO - Journal of Alzheimer's Disease

JF - Journal of Alzheimer's Disease

SN - 1387-2877

IS - 3

ER -

Elevated Pure Tone Thresholds Are Associated with Altered Microstructure in Cortical Areas Related to Auditory Processing and Attentional Allocation

Abstract

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