Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss
Abstract
Background Patients with age-related hearing loss (ARHL) often struggle with tracking and locating sound sources, but the neural signature associated with these impairments remains unclear. Materials and methods Using a passive listening task with stimuli from five different horizontal directions in functional magnetic resonance imaging, we defined functional regions of interest (ROIs) of the auditory “where” pathway based on the data of previous literatures and young normal hearing listeners ( n = 20). Then, we investigated associations of the demographic, cognitive, and behavioral features of sound localization with task-based activation and connectivity of the ROIs in ARHL patients ( n = 22). Results We found that the increased high-level region activation, such as the premotor cortex and inferior parietal lobule, was associated with increased localization accuracy and cognitive function. Moreover, increased connectivity between the left planum temporale and left superior frontal gyrus was associated with increased localization accuracy in ARHL. Increased connectivity between right primary auditory cortex and right middle temporal gyrus, right premotor cortex and left anterior cingulate cortex, and right planum temporale and left lingual gyrus in ARHL was associated with decreased localization accuracy. Among the ARHL patients, the task-dependent brain activation and connectivity of certain ROIs were associated withmore »
- Authors:
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research
- OSTI Identifier:
- 2325537
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Neuroscience (Online)
- Additional Journal Information:
- Journal Name: Frontiers in Neuroscience (Online) Journal Volume: 18; Journal ID: ISSN 1662-453X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
Citation Formats
Wu, Junzhi, Nie, Shuai, Li, Chunlin, Wang, Xing, Peng, Ye, Shang, Jiaqi, Diao, Linan, Ding, Hongping, Si, Qian, Wang, Songjian, Tong, Renjie, Li, Yutang, Sun, Liwei, and Zhang, Juan. Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss. Switzerland: N. p., 2024.
Web. doi:10.3389/fnins.2024.1353413.
Wu, Junzhi, Nie, Shuai, Li, Chunlin, Wang, Xing, Peng, Ye, Shang, Jiaqi, Diao, Linan, Ding, Hongping, Si, Qian, Wang, Songjian, Tong, Renjie, Li, Yutang, Sun, Liwei, & Zhang, Juan. Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss. Switzerland. https://doi.org/10.3389/fnins.2024.1353413
Wu, Junzhi, Nie, Shuai, Li, Chunlin, Wang, Xing, Peng, Ye, Shang, Jiaqi, Diao, Linan, Ding, Hongping, Si, Qian, Wang, Songjian, Tong, Renjie, Li, Yutang, Sun, Liwei, and Zhang, Juan. Mon .
"Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss". Switzerland. https://doi.org/10.3389/fnins.2024.1353413.
@article{osti_2325537,
title = {Sound-localization-related activation and functional connectivity of dorsal auditory pathway in relation to demographic, cognitive, and behavioral characteristics in age-related hearing loss},
author = {Wu, Junzhi and Nie, Shuai and Li, Chunlin and Wang, Xing and Peng, Ye and Shang, Jiaqi and Diao, Linan and Ding, Hongping and Si, Qian and Wang, Songjian and Tong, Renjie and Li, Yutang and Sun, Liwei and Zhang, Juan},
abstractNote = {Background Patients with age-related hearing loss (ARHL) often struggle with tracking and locating sound sources, but the neural signature associated with these impairments remains unclear. Materials and methods Using a passive listening task with stimuli from five different horizontal directions in functional magnetic resonance imaging, we defined functional regions of interest (ROIs) of the auditory “where” pathway based on the data of previous literatures and young normal hearing listeners ( n = 20). Then, we investigated associations of the demographic, cognitive, and behavioral features of sound localization with task-based activation and connectivity of the ROIs in ARHL patients ( n = 22). Results We found that the increased high-level region activation, such as the premotor cortex and inferior parietal lobule, was associated with increased localization accuracy and cognitive function. Moreover, increased connectivity between the left planum temporale and left superior frontal gyrus was associated with increased localization accuracy in ARHL. Increased connectivity between right primary auditory cortex and right middle temporal gyrus, right premotor cortex and left anterior cingulate cortex, and right planum temporale and left lingual gyrus in ARHL was associated with decreased localization accuracy. Among the ARHL patients, the task-dependent brain activation and connectivity of certain ROIs were associated with education, hearing loss duration, and cognitive function. Conclusion Consistent with the sensory deprivation hypothesis, in ARHL, sound source identification, which requires advanced processing in the high-level cortex, is impaired, whereas the right–left discrimination, which relies on the primary sensory cortex, is compensated with a tendency to recruit more resources concerning cognition and attention to the auditory sensory cortex. Overall, this study expanded our understanding of the neural mechanisms contributing to sound localization deficits associated with ARHL and may serve as a potential imaging biomarker for investigating and predicting anomalous sound localization.},
doi = {10.3389/fnins.2024.1353413},
journal = {Frontiers in Neuroscience (Online)},
number = ,
volume = 18,
place = {Switzerland},
year = {Mon Mar 18 00:00:00 EDT 2024},
month = {Mon Mar 18 00:00:00 EDT 2024}
}
https://doi.org/10.3389/fnins.2024.1353413
Works referenced in this record:
Brain correlates of the orientation of auditory spatial attention onto speaker location in a “cocktail‐party” situation
journal, June 2016
- Lewald, Jörg; Hanenberg, Christina; Getzmann, Stephan
- Psychophysiology, Vol. 53, Issue 10
The Contribution of the Inferior Parietal Lobe to Auditory Spatial Working Memory
journal, February 2008
- Alain, Claude; He, Yu; Grady, Cheryl
- Journal of Cognitive Neuroscience, Vol. 20, Issue 2
Proficiency in Using Level Cue for Sound Localization Is Related to the Auditory Cortical Structure in Patients With Single-Sided Deafness
journal, October 2021
- Kim, Ja Hee; Shim, Leeseul; Bahng, Junghwa
- Frontiers in Neuroscience, Vol. 15
Processing of sound location in human cortex
journal, March 2008
- Lewald, Jörg; Riederer, Klaus A. J.; Lentz, Tobias
- European Journal of Neuroscience, Vol. 27, Issue 5
Conn : A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks
journal, June 2012
- Whitfield-Gabrieli, Susan; Nieto-Castanon, Alfonso
- Brain Connectivity, Vol. 2, Issue 3
Somatosensory Cross-Modal Reorganization in Adults With Age-Related, Early-Stage Hearing Loss
journal, May 2018
- Cardon, Garrett; Sharma, Anu
- Frontiers in Human Neuroscience, Vol. 12
At the interface of sensory and motor dysfunctions and Alzheimer's disease
journal, January 2015
- Albers, Mark W.; Gilmore, Grover C.; Kaye, Jeffrey
- Alzheimer's & Dementia, Vol. 11, Issue 1
“What” and “where” in the human auditory system
journal, September 2001
- Alain, Claude; Arnott, Stephen R.; Hevenor, Stephanie
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 21
Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015
journal, October 2016
- Vos, Theo; Allen, Christine; Arora, Megha
- The Lancet, Vol. 388, Issue 10053
Evidence of a functional reorganization in the auditory dorsal stream following unilateral hearing loss
journal, December 2020
- Vannson, Nicolas; Strelnikov, Kuzma; James, Chris J.
- Neuropsychologia, Vol. 149
Functional Connectivity of Heschl’s Gyrus Associated With Age-Related Hearing Loss: A Resting-State fMRI Study
journal, November 2019
- Fitzhugh, Megan C.; Hemesath, Angela; Schaefer, Sydney Y.
- Frontiers in Psychology, Vol. 10
Active Sound Localization Sharpens Spatial Tuning in Human Primary Auditory Cortex
journal, August 2018
- van der Heijden, Kiki; Rauschecker, Josef P.; Formisano, Elia
- The Journal of Neuroscience, Vol. 38, Issue 40
Generalizable representations of pain, cognitive control, and negative emotion in medial frontal cortex
journal, January 2018
- Kragel, Philip A.; Kano, Michiko; Van Oudenhove, Lukas
- Nature Neuroscience, Vol. 21, Issue 2
Mechanisms of Sound Localization in Two Functionally Distinct Regions of the Auditory Cortex
journal, December 2015
- Razak, Khaleel A.; Yarrow, Stuart; Brewton, Dustin
- The Journal of Neuroscience, Vol. 35, Issue 49
Are age-related changes in cognitive function driven by age-related changes in sensory processing?
journal, December 2012
- Humes, Larry E.; Busey, Thomas A.; Craig, James
- Attention, Perception, & Psychophysics, Vol. 75, Issue 3
Construct Validity of the Stroop Color-Word Test: Influence of Speed of Visual Search, Verbal Fluency, Working Memory, Cognitive Flexibility, and Conflict Monitoring
journal, June 2020
- Periáñez, José A.; Lubrini, Genny; García-Gutiérrez, Ana
- Archives of Clinical Neuropsychology, Vol. 36, Issue 1
The effects of age and cochlear hearing loss on temporal fine structure sensitivity, frequency selectivity, and speech reception in noise
journal, July 2011
- Hopkins, Kathryn; Moore, Brian C. J.
- The Journal of the Acoustical Society of America, Vol. 130, Issue 1
The Neuroanatomy of Speech Processing: A Large-scale Lesion Study
journal, June 2022
- Rogalsky, Corianne; Basilakos, Alexandra; Rorden, Chris
- Journal of Cognitive Neuroscience
Abnormal Neural Filtering of Irrelevant Visual Information in Depression
journal, February 2009
- Desseilles, Martin; Balteau, Evelyne; Sterpenich, Virginie
- The Journal of Neuroscience, Vol. 29, Issue 5
The Speech, Spatial and Qualities of Hearing Scale (SSQ)
journal, January 2004
- Gatehouse, Stuart; Noble, William
- International Journal of Audiology, Vol. 43, Issue 2
Central Auditory Dysfunction in Older Persons With Memory Impairment or Alzheimer Dementia
journal, July 2008
- Gates, George A.; Anderson, Melissa L.; Feeney, M. Patrick
- Archives of Otolaryngology–Head & Neck Surgery, Vol. 134, Issue 7
Left frontal eye field encodes sound locations during passive listening
journal, July 2022
- Sun, Liwei; Li, Chunlin; Wang, Songjian
- Cerebral Cortex, Vol. 33, Issue 6
High Binaural Coherence Determines Successful Sound Localization and Increased Activity in Posterior Auditory Areas
journal, September 2005
- Zimmer, U.; Macaluso, E.
- Neuron, Vol. 47, Issue 6
How do aging and age-related hearing loss affect the ability to communicate effectively in challenging communicative conditions?
journal, November 2018
- Hazan, Valerie; Tuomainen, Outi; Tu, Lilian
- Hearing Research, Vol. 369
Socioeconomic and lifestyle factors associated with hearing loss in older adults: a cross-sectional study of the English Longitudinal Study of Ageing (ELSA)
journal, September 2019
- Tsimpida, Dialechti; Kontopantelis, Evangelos; Ashcroft, Darren
- BMJ Open, Vol. 9, Issue 9
The effect of brain lesions on sound localization in complex acoustic environments
journal, March 2014
- Zündorf, Ida C.; Karnath, Hans-Otto; Lewald, Jörg
- Brain, Vol. 137, Issue 5
American Geriatrics Society and National Institute on Aging Bench‐to‐Bedside Conference: Sensory Impairment and Cognitive Decline in Older Adults
journal, September 2018
- Whitson, Heather E.; Cronin‐Golomb, Alice; Cruickshanks, Karen J.
- Journal of the American Geriatrics Society, Vol. 66, Issue 11
Modeling the Effects of Sensorineural Hearing Loss on Sound Localization in the Median Plane
journal, January 2016
- Baumgartner, Robert; Majdak, Piotr; Laback, Bernhard
- Trends in Hearing, Vol. 20
Presbycusis Disrupts Spontaneous Activity Revealed by Resting-State Functional MRI
journal, March 2018
- Chen, Yu-Chen; Chen, Huiyou; Jiang, Liang
- Frontiers in Behavioral Neuroscience, Vol. 12
Assessing the auditory dual-pathway model in humans
journal, May 2004
- Arnott, Stephen R.; Binns, Malcolm A.; Grady, Cheryl L.
- NeuroImage, Vol. 22, Issue 1
Self-reported experiences of discrimination in older black adults are associated with insula functional connectivity
journal, July 2020
- Han, S. Duke; Lamar, Melissa; Fleischman, Debra
- Brain Imaging and Behavior, Vol. 15, Issue 4
Effective connectivity analysis demonstrates involvement of premotor cortex during speech perception
journal, February 2011
- Osnes, Berge; Hugdahl, Kenneth; Specht, Karsten
- NeuroImage, Vol. 54, Issue 3
Brain imaging evidence of preclinical Alzheimer's disease in normal aging
journal, February 2006
- Jagust, William; Gitcho, Amy; Sun, Felice
- Annals of Neurology, Vol. 59, Issue 4
Aberrant brain functional hubs and causal connectivity in presbycusis
journal, September 2020
- Xing, Chunhua; Chen, Yu-Chen; Tong, Zhaopeng
- Brain Imaging and Behavior, Vol. 15, Issue 1
Evidence for distinct human auditory cortex regions for sound location versus identity processing
journal, October 2013
- Ahveninen, Jyrki; Huang, Samantha; Nummenmaa, Aapo
- Nature Communications, Vol. 4, Issue 1
An fMRI study of the Trail Making Test
journal, January 2005
- Zakzanis, Konstantine K.; Mraz, Richard; Graham, Simon J.
- Neuropsychologia, Vol. 43, Issue 13
Brain networks involved in haptic and visual identification of facial expressions of emotion: An fMRI study
journal, January 2010
- Kitada, Ryo; Johnsrude, Ingrid S.; Kochiyama, Takanori
- NeuroImage, Vol. 49, Issue 2
de Bruijn cycles for neural decoding
journal, June 2011
- Aguirre, Geoffrey Karl; Mattar, Marcelo Gomes; Magis-Weinberg, Lucía
- NeuroImage, Vol. 56, Issue 3
Cognitive reserve and brain maintenance in aging and dementia: An integrative review
journal, January 2021
- Alvares Pereira, Gabriela; Silva Nunes, Maria Vânia; Alzola, Patricia
- Applied Neuropsychology: Adult, Vol. 29, Issue 6
Disrupted Functional Network Connectivity Predicts Cognitive Impairment in Presbycusis Patients
journal, August 2020
- Xing, Chunhua; Zhang, Juan; Cui, Jinluan
- Frontiers in Aging Neuroscience, Vol. 12
Cortical Correlates of Binaural Temporal Processing Deficits in Older Adults
journal, May 2018
- Eddins, Ann Clock; Eddins, David A.
- Ear & Hearing, Vol. 39, Issue 3
The Neural Consequences of Age-Related Hearing Loss
journal, July 2016
- Peelle, Jonathan E.; Wingfield, Arthur
- Trends in Neurosciences, Vol. 39, Issue 7
The grounding of abstract concepts in the motor and visual system: An fMRI study
journal, March 2020
- Harpaintner, Marcel; Sim, Eun-Jin; Trumpp, Natalie M.
- Cortex, Vol. 124
Changed crossmodal functional connectivity in older adults with hearing loss
journal, January 2017
- Puschmann, Sebastian; Thiel, Christiane M.
- Cortex, Vol. 86
Enhanced Sound Localization
journal, June 2004
- Mungamuru, B.; Aarabi, P.
- IEEE Transactions on Systems, Man and Cybernetics, Part B (Cybernetics), Vol. 34, Issue 3
Association between Exposure to the Chinese Famine in Different Stages of Early Life and Decline in Cognitive Functioning in Adulthood
journal, July 2016
- Wang, Chao; An, Yu; Yu, Huanling
- Frontiers in Behavioral Neuroscience, Vol. 10
Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study
journal, October 2001
- Maeder, Philippe P.; Meuli, Reto A.; Adriani, Michela
- NeuroImage, Vol. 14, Issue 4
Dementia prevention, intervention, and care
journal, December 2017
- Livingston, Gill; Sommerlad, Andrew; Orgeta, Vasiliki
- The Lancet, Vol. 390, Issue 10113
Representation of Auditory Motion Directions and Sound Source Locations in the Human Planum Temporale
journal, January 2019
- Battal, Ceren; Rezk, Mohamed; Mattioni, Stefania
- The Journal of Neuroscience, Vol. 39, Issue 12
Hearing Loss and Incident Dementia
journal, February 2011
- Lin, Frank R.; Metter, E. Jeffrey; O’Brien, Richard J.
- Archives of Neurology, Vol. 68, Issue 2
Tuning to Binaural Cues in Human Auditory Cortex
journal, October 2015
- McLaughlin, Susan A.; Higgins, Nathan C.; Stecker, G. Christopher
- Journal of the Association for Research in Otolaryngology, Vol. 17, Issue 1
Testing the dual-pathway model for auditory processing in human cortex
journal, January 2016
- Zündorf, Ida C.; Lewald, Jörg; Karnath, Hans-Otto
- NeuroImage, Vol. 124
Cortical mechanisms of spatial hearing
journal, August 2019
- van der Heijden, Kiki; Rauschecker, Josef P.; de Gelder, Beatrice
- Nature Reviews Neuroscience, Vol. 20, Issue 10
Where is 'where' in the human auditory cortex?
journal, August 2002
- Zatorre, Robert J.; Bouffard, Marc; Ahad, Pierre
- Nature Neuroscience, Vol. 5, Issue 9
Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey
journal, January 2000
- Lewis, James W.; Van Essen, David C.
- The Journal of Comparative Neurology, Vol. 428, Issue 1
Age-related Hearing Loss and Ear Morphology Affect Vertical but not Horizontal Sound-Localization Performance
journal, January 2013
- Otte, Rik J.; Agterberg, Martijn J. H.; Van Wanrooij, Marc M.
- Journal of the Association for Research in Otolaryngology, Vol. 14, Issue 2
Research Insights on Neural Effects of Auditory Deprivation and Restoration in Unilateral Hearing Loss: A Systematic Review
journal, March 2020
- Vanderauwera, Jolijn; Hellemans, Elisabeth; Verhaert, Nicolas
- Journal of Clinical Medicine, Vol. 9, Issue 3
Domain-general subregions of the medial prefrontal cortex contribute to recovery of language after stroke
journal, June 2017
- Geranmayeh, Fatemeh; Chau, Tsz Wing; Wise, Richard J. S.
- Brain, Vol. 140, Issue 7
Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders
journal, December 2013
- Arenaza-Urquijo, Eider M.; Landeau, Brigitte; La Joie, Renaud
- NeuroImage, Vol. 83
Patients with mild cognitive impairment have an abnormal upper-alpha event-related desynchronization/synchronization (ERD/ERS) during a task of temporal attention
journal, June 2014
- Caravaglios, Giuseppe; Muscoso, Emma Gabriella; Di Maria, Giulia
- Journal of Neural Transmission, Vol. 122, Issue 3
Abnormal Static and Dynamic Functional Network Connectivity in Patients With Presbycusis
journal, January 2022
- Xing, Chunhua; Chen, Yu-Chen; Shang, Song’an
- Frontiers in Aging Neuroscience, Vol. 13
Increased activity in frontal motor cortex compensates impaired speech perception in older adults
journal, August 2016
- Du, Yi; Buchsbaum, Bradley R.; Grady, Cheryl L.
- Nature Communications, Vol. 7, Issue 1
The Effects of Age-Related Hearing Loss on the Brain and Cognitive Function
journal, October 2020
- Slade, Kate; Plack, Christopher J.; Nuttall, Helen E.
- Trends in Neurosciences, Vol. 43, Issue 10
Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex
journal, December 1999
- Romanski, L. M.; Tian, B.; Fritz, J.
- Nature Neuroscience, Vol. 2, Issue 12