Spatial selective auditory attention is preserved in older age but is degraded by peripheral hearing loss.
Ageing
Attention
Hearing
Speech perception
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
31 Oct 2024
31 Oct 2024
Historique:
received:
23
04
2024
accepted:
18
10
2024
medline:
1
11
2024
pubmed:
1
11
2024
entrez:
1
11
2024
Statut:
epublish
Résumé
Interest in how ageing affects attention is long-standing, although interactions between sensory and attentional processing in older age are not fully understood. Here, we examined interactions between peripheral hearing and selective attention in a spatialised cocktail party listening paradigm, in which three talkers spoke different sentences simultaneously and participants were asked to report the sentence spoken by a talker at a particular location. By comparing a sample of older (N = 61; age = 55-80 years) and younger (N = 58; age = 18-35 years) adults, we show that, as a group, older adults benefit as much as younger adults from preparatory spatial attention. Although, for older adults, this benefit significantly reduces with greater age-related hearing loss. These results demonstrate that older adults with excellent hearing retain the ability to direct spatial selective attention, but this ability deteriorates, in a graded manner, with age-related hearing loss. Thus, reductions in spatial selective attention likely contribute to difficulties communicating in social settings for older adults with age-related hearing loss. Overall, these findings demonstrate a relationship between mild perceptual decline and attention in older age.
Identifiants
pubmed: 39482327
doi: 10.1038/s41598-024-77102-5
pii: 10.1038/s41598-024-77102-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26243Subventions
Organisme : Wellcome Trust
ID : 203147/Z/16/Z
Pays : United Kingdom
Organisme : Royal National Institute for Deaf People
ID : PA25_Holmes
Informations de copyright
© 2024. The Author(s).
Références
Veríssimo, J., Verhaeghen, P., Goldman, N., Weinstein, M. & Ullman, M. T. Evidence that ageing yields improvements as well as declines across attention and executive functions. Nat. Hum. Behav. 6, 97–110 (2021).
Craik, F. I. M. & Salthouse, T, A. The Handbook of Aging and Cognition (Psychology, 2008).
Gottlob, L. R. & Madden, D. J. Time course of allocation of visual attention after equating for sensory differences: An age-related perspective. Psychol. Aging 13, 138–149 (1998).
pubmed: 9533196
doi: 10.1037/0882-7974.13.1.138
Hartley, A. A., Kieley, J. M. & Slabach, E. H. Age differences and similarities in the effects of cues and prompts. J. Exp. Psychol. Hum. Percept. Perform. 16, 523–537 (1990).
pubmed: 2144568
doi: 10.1037/0096-1523.16.3.523
Nissen, M. J. & Corkin, S. Effectiveness of attentional cueing in older and younger adults. J. Gerontol. 40, 185–191 (1985).
pubmed: 3973359
doi: 10.1093/geronj/40.2.185
Humes, L. E. Factors underlying individual differences in speech-recognition threshold (SRT) in noise among older adults. Front. Aging Neurosci. 13, 702739 (2021).
pubmed: 34290600
pmcid: 8287901
doi: 10.3389/fnagi.2021.702739
Murphy, D. R., Daneman, M. & Schneider, B. A. Why do older adults have difficulty following conversations? Psychol. Aging 21, 49–61 (2006).
pubmed: 16594791
doi: 10.1037/0882-7974.21.1.49
Summerfield, C. & Egner, T. Expectation (and attention) in visual cognition. Trends Cogn. Sci. 13, 403–409 (2009).
pubmed: 19716752
doi: 10.1016/j.tics.2009.06.003
Zanto, T. P. & Gazzaley, A. Attention and ageing. In The Oxford Handbook of Attention (eds Nobre, A. C. & Kastner, S.) (Oxford University Press, 2014). https://doi.org/10.1093/oxfordhb/9780199675111.013.020 .
Killeen, O. J., Zhou, Y. & Ehrlich, J. R. Objectively measured visual impairment and dementia prevalence in older adults in the US. JAMA Ophthalmol. 141, 786–790 (2023).
pubmed: 37440238
pmcid: 10346499
doi: 10.1001/jamaophthalmol.2023.2854
Griffiths, T. D. et al. How can hearing loss cause dementia? Neuron 108, 401–412 (2020).
pubmed: 32871106
pmcid: 7664986
doi: 10.1016/j.neuron.2020.08.003
Lin, F. R. et al. Hearing loss and incident dementia. Arch. Neurol. 68, 214–220 (2011).
pubmed: 21320988
pmcid: 3277836
doi: 10.1001/archneurol.2010.362
Holmes, E. & Griffiths, T. D. Normal’ hearing thresholds and fundamental auditory grouping processes predict difficulties with speech-in-noise perception. Sci. Rep. 9, 16771 (2019).
pubmed: 31728002
pmcid: 6856372
doi: 10.1038/s41598-019-53353-5
Humes, L. E., Kidd, G. R. & Lentz, J. J. Auditory and cognitive factors underlying individual differences in aided speech-understanding among older adults. Front. Syst. Neurosci. 7, 55 (2013).
pubmed: 24098273
pmcid: 3787592
doi: 10.3389/fnsys.2013.00055
Jerger, J., Jerger, S., Oliver, T. & Pirozzolo, F. Speech understanding in the elderly. Ear Hear. 10, 79–89 (1989).
pubmed: 2707505
doi: 10.1097/00003446-198904000-00001
Lentz, J. J., Humes, L. E. & Kidd, G. R. Differences in auditory perception between young and older adults when controlling for differences in hearing loss and cognition. Trends Hear. 26 (2022).
van Rooij, J. C. G. M. & Plomp, R. Auditive and cognitive factors in speech perception by elderly listeners. III. Additional data and final discussion. J. Acoust. Soc. Am. 91, 1028–1033 (1992).
pubmed: 1556304
doi: 10.1121/1.402628
Wingfield, A. & Tun, P. A. Spoken language comprehension in older adults: Interactions between sensory and cognitive change in normal aging. Semin. Hear. 22, 287–301 (2001).
doi: 10.1055/s-2001-15632
Helfer, K. S. & Freyman, R. L. Stimulus and listener factors affecting age-related changes in competing speech perception. J. Acoust. Soc. Am. 136, 748 (2014).
pubmed: 25096109
pmcid: 4187459
doi: 10.1121/1.4887463
Goossens, T., Vercammen, C., Wouters, J. & van Wieringen, A. Masked speech perception across the adult lifespan: Impact of age and hearing impairment. Hear. Res. 344, 109–124 (2017).
pubmed: 27845259
doi: 10.1016/j.heares.2016.11.004
Petersen, S. & Posner, M. I. The attention system of the human brain: 20 years after. Annu. Rev. Neurosci. 21, 73–89 (2012).
doi: 10.1146/annurev-neuro-062111-150525
Holmes, E., Kitterick, P. T. & Summerfield, A. Q. Cueing listeners to attend to a target talker progressively improves word report as the duration of the cue-target interval lengthens to 2,000 ms. Atten. Percept. Psychophys. 80, 1520–1538 (2018).
pubmed: 29696570
doi: 10.3758/s13414-018-1531-x
Koch, I., Lawo, V., Fels, J. & Vorländer, M. Switching in the cocktail party: Exploring intentional control of auditory selective attention. J. Exp. Psychol. Hum. Percept. Perform. 37, 1140–1147 (2011).
pubmed: 21553997
doi: 10.1037/a0022189
Hill, K. T. & Miller, L. M. Auditory attentional control and selection during cocktail party listening. Cereb. Cortex 20, 583–590 (2010).
pubmed: 19574393
doi: 10.1093/cercor/bhp124
Holmes, E., Kitterick, P. T. & Summerfield, A. Q. EEG activity evoked in preparation for multi-talker listening by adults and children. Hear. Res. 336, 83–100 (2016).
pubmed: 27178442
doi: 10.1016/j.heares.2016.04.007
Giesbrecht, B., Weissman, D. H., Woldorff, M. G. & Mangun, G. R. Pre-target activity in visual cortex predicts behavioral performance on spatial and feature attention tasks. Brain Res. 1080, 63–72 (2006).
pubmed: 16412994
doi: 10.1016/j.brainres.2005.09.068
Best, V., Marrone, N., Mason, C. R., Kidd, G. & Shinn-Cunningham, B. G. Effects of sensorineural hearing loss on visually guided attention in a multitalker environment. J. Assoc. Res. Otolaryngol. 10, 142–149 (2009).
pubmed: 19009321
doi: 10.1007/s10162-008-0146-7
Holmes, E., Kitterick, P. T. & Summerfield, A. Q. Peripheral hearing loss reduces the ability of children to direct selective attention during multi-talker listening. Hear. Res. 350, 160–172 (2017).
pubmed: 28505526
doi: 10.1016/j.heares.2017.05.005
Glick, H. & Sharma, A. Cross-modal plasticity in developmental and age-related hearing loss: Clinical implications. Hear. Res. 343, 191–201 (2017).
pubmed: 27613397
doi: 10.1016/j.heares.2016.08.012
Mehraei, G., Gallun, F. J., Leek, M. R. & Bernstein, J. G. W. Spectrotemporal modulation sensitivity for hearing-impaired listeners: Dependence oncarrier center frequency and the relationship to speech intelligibility. J. Acoust. Soc. Am. 136, 301 (2014).
pubmed: 24993215
pmcid: 4187385
doi: 10.1121/1.4881918
Trujillo, M. & Razak, K. A. Altered cortical spectrotemporal processing with age-related hearing loss. J. Neurophysiol. 110, 2873–2886 (2013).
pubmed: 24068755
doi: 10.1152/jn.00423.2013
Bernstein, J. G. W. et al. Spectrotemporal modulation sensitivity as a predictor of speech intelligibility for hearing-impaired listeners. J. Am. Acad. Audiol.24, 293–306 (2013).
pubmed: 23636210
pmcid: 3973426
doi: 10.3766/jaaa.24.4.5
Eddins, A. C., Ozmeral, E. J. & Eddins, D. A. How aging impacts the encoding of binaural cues and the perception of auditory space. Hear. Res. 369, 79–89 (2018).
pubmed: 29759684
pmcid: 6196106
doi: 10.1016/j.heares.2018.05.001
Moore, B. C. J. Cochlear Hearing Loss: Physiological, Psychological and Technical Issues (Wiley, 2007).
Dai, L., Best, V. & Shinn-Cunningham, B. G. Sensorineural hearing loss degrades behavioral and physiological measures of human spatial selective auditory attention. Proc. Natl. Acad. Sci. 115, E3286–E3295 (2018).
pubmed: 29555752
pmcid: 5889663
doi: 10.1073/pnas.1721226115
Ozmeral, E. J., Eddins, D. A. & Eddins, A. C. Selective auditory attention modulates cortical responses to sound location change in younger and older adults. J. Neurophysiol. 126, 803–815 (2021).
pubmed: 34288759
pmcid: 8461830
doi: 10.1152/jn.00609.2020
Akeroyd, M. A. & Whitmer, W. M. Spatial hearing and hearing aids. ENT Audiol. News 20, 76 (2011).
pubmed: 24109504
pmcid: 3791412
Willott, J. F. Anatomic and physiologic aging: A behavioral neuroscience perspective. J. Am. Acad. Audiol. 7, 141–151 (1996).
pubmed: 8780986
Presacco, A., Simon, J. Z. & Anderson, S. Speech-in-noise representation in the aging midbrain and cortex: Effects of hearing loss. PLoS One 14, 1–26 (2019).
doi: 10.1371/journal.pone.0213899
Wolak, T. et al. Altered functional connectivity in patients with sloping Sensorineural hearing loss. Front. Hum. Neurosci. 13, 459450 (2019).
doi: 10.3389/fnhum.2019.00284
Peelle, J. E., Troiani, V., Grossman, M. & Wingfield, A. Hearing loss in older adults affects neural systems supporting speech comprehension. J. Neurosci. 31, 12638–12643 (2011).
pubmed: 21880924
pmcid: 3175595
doi: 10.1523/JNEUROSCI.2559-11.2011
Humes, L. E. et al. Central presbycusis: A review and evaluation of the evidence. J. Am. Acad. Audiol. 23, 635–666. https://doi.org/10.3766/jaaa.23.8.5 (2012).
Schneider, B. A., Daneman, M., Murphy, D. R. & See, S. K. Listening to discourse in distracting settings: The effects of aging. Psychol. Aging 15, 110–125 (2000).
pubmed: 10755294
doi: 10.1037/0882-7974.15.1.110
Schneider, B. A., Daneman, M. & Pichora-Fuller, M. K. Listening in aging adults: From discourse comprehension to psychoacoustics. Can. J. Exp. Psychol. 56, 139–152 (2002).
pubmed: 12271745
doi: 10.1037/h0087392
Wingfield, A., Tun, P. A., Mccoy, S. L. & Mccoy, L. Hearing loss in older adulthood: What it is and how it interacts with cognitive performance 14, 144–148 (2014).
Pichora-Fuller, M. K. Use of supportive context by younger and older adult listeners: Balancing bottom-up and top-down information processing. Int. J. Audiol. 47, 1708–8186 (2008).
Dryden, A., Allen, H. A., Henshaw, H. & Heinrich, A. The Association between Cognitive Performance and Speech-in-noise perception for adult listeners: A systematic literature review and Meta-analysis. Trends Hear. 21, 233121651774467 (2017).
Akeroyd, M. A. Are individual differences in speech reception related to individual differences in cognitive ability? A survey of twenty experimental studies with normal and hearing-impaired adults. Int. J. Audiol. 47(Suppl 2), S53–S71 (2008).
pubmed: 19012113
doi: 10.1080/14992020802301142
Cattell, R. B. Theory of fluid and crystallized intelligence: A critical experiment. J. Educ. Psychol. 54, 1–22 (1963).
doi: 10.1037/h0046743
Pichora-Fuller, M. K., Schneider, B. A. & Daneman, M. How young and old adults listen to and remember speech in noise. J. Acoust. Soc. Am. 97, 593–608 (1995).
pubmed: 7860836
doi: 10.1121/1.412282
Schneider, B. A. & Pichora-Fuller, M. K. Age-related changes in temporal processing: Implications for speech perception. Semin Hear. 22, 227–238 (2001).
doi: 10.1055/s-2001-15628
Wechsler, D. Wechsler Adult Intelligence scale–Fourth Edition (WAIS–IV) (NCS Pearson, 2008).
Helfer, K. S. Competing speech perception in middle age. Am. J. Audiol. 24, 80 (2015).
pubmed: 25768264
pmcid: 4567969
doi: 10.1044/2015_AJA-14-0056
Helfer, K. S., Merchant, G. R. & Wasiuk, P. A. Age-related changes in objective and subjective Speech Perception in Complex listening environments. J. Speech Lang. Hear. Res. 60, 3009 (2017).
pubmed: 29049601
pmcid: 5945070
doi: 10.1044/2017_JSLHR-H-17-0030
Folk, C. L. & Hoyer, W. J. Aging and shifts of visual spatial attention. Psychol. Aging 7, 453–465 (1992).
pubmed: 1388867
doi: 10.1037/0882-7974.7.3.453
Lincourt, A. E., Folk, C. L. & Hoyer, W. J. Effects of aging on voluntary and involuntary shifts of attention. Aging Neuropsychol. Cogn. 4, 290–303 (1997).
doi: 10.1080/13825589708256654
Olk, B. & Kingstone, A. Attention and ageing: Measuring effects of involuntary and voluntary orienting in isolation and in combination. Br. J. Psychol. 106, 235–252 (2015).
pubmed: 25040206
doi: 10.1111/bjop.12082
Fozard, J. L., Vercruyssen, M., Reynolds, S. L., Hancock, P. A. & Quilter, R. E. Age differences and changes in reaction time: The Baltimore Longitudinal Study of Aging. J. Gerontol. 49 (1994).
Hardwick, R. M., Forrence, A. D., Costello, G., Zackowski, M., Haith, A. M. & K. & Control of Movement: Age-related increases in reaction time result from slower preparation, not delayed initiation. J. Neurophysiol. 128, 582 (2022).
pubmed: 35829640
pmcid: 9423772
doi: 10.1152/jn.00072.2022
Ebaid, D. & Crewther, S. G. Time for a systems biological approach to cognitive aging?—A critical review. Front. Aging Neurosci. https://doi.org/10.3389/fnagi.2020.00114 (2020).
doi: 10.3389/fnagi.2020.00114
Humes, L. E., Busey, T. A., Craig, J. & Kewley-Port, D. Are age-related changes in cognitive function driven by age-related changes in sensory processing? Atten. Percept. Psychophys. 75, 508–524 (2013).
pubmed: 23254452
doi: 10.3758/s13414-012-0406-9
Stevenson, J. S., Clifton, L., Kuźma, E. & Littlejohns, T. J. Speech-in‐noise hearing impairment is associated with an increased risk of incident dementia in 82,039 UK Biobank participants. Alzheimer’s Dement. 12416. https://doi.org/10.1002/ALZ.12416 (2021).
Gatehouse, S. & Akeroyd, M. A. The effects of cueing temporal and spatial attention on word recognition in a complex listening task in hearing-impaired listeners. Trends Amplif. 12, 145–161 (2008).
pubmed: 18567595
pmcid: 4111433
doi: 10.1177/1084713808317395
Rosemann, S. & Thiel, C. M. Neuroanatomical changes associated with age-related hearing loss and listening effort. Brain Struct. Funct. 225, 2689–2700 (2020).
pubmed: 32960318
pmcid: 7674350
doi: 10.1007/s00429-020-02148-w
Slade, K. et al. The impact of age-related hearing loss on structural neuroanatomy: A meta-analysis. Front. Neurol. 13, 1703 (2022).
doi: 10.3389/fneur.2022.950997
Butler, B. E., Sunstrum, J. K. & Lomber, S. G. Modified origins of cortical projections to the superior colliculus in the deaf: Dispersion of auditory efferents. J. Neurosci. 38, 2858–2817 (2018).
doi: 10.1523/JNEUROSCI.2858-17.2018
Rönnberg, J. et al. The ease of Language understanding (ELU) model: Theoretical, empirical, and clinical advances. Front. Syst. Neurosci. 7, 31 (2013).
pubmed: 23874273
pmcid: 3710434
doi: 10.3389/fnsys.2013.00031
Wingfield, A., Tun, P. A. & McCoy, S. L. Hearing loss in older adulthood: What it is and how it interacts with cognitive performance. Curr. Dir. Psychol. Sci. 14, 144–148 (2005).
doi: 10.1111/j.0963-7214.2005.00356.x
Murphy, G., Groeger, J. A. & Greene, C. M. Twenty years of load theory—Where are we now, and where should we go next? Psychon. Bull. Rev. 23, 1316–1340 (2016).
Rosemann, S. & Thiel, C. M. The effect of age-related hearing loss and listening effort on resting state connectivity. Sci. Rep. 9, 2337 (2019).
pubmed: 30787339
pmcid: 6382886
doi: 10.1038/s41598-019-38816-z
Heinrich, A. & Schneider, B. A. Elucidating the effects of ageing on remembering perceptually distorted word pairs 64, 186–205. https://doi.org/10.1080/17470218.2010.492621 (2011).
Schneider, W. & Shiffrin, R. M. Controlled and automatic human information processing: I. Detection, search, and attention. Psychol. Rev. 84, 1–66 (1977).
doi: 10.1037/0033-295X.84.1.1
Holmes, E., Folkeard, P., Johnsrude, I. S. & Scollie, S. Semantic context improves speech intelligibility and reduces listening effort for listeners with hearing impairment. Int. J. Audiol. 57, 483–492 (2018).
pubmed: 29415585
doi: 10.1080/14992027.2018.1432901
Heinrich, A. The role of cognition for speech-in-noise perception: Considering individual listening strategies related to aging and hearing loss. Int. J. Behav. Dev. 45, 382–388 (2020).
doi: 10.1177/0165025420914984
Rönnberg, J., Holmer, E. & Rudner, M. Cognitive hearing science and ease of language understanding. 58, 247–261. https://doi.org/10.1080/14992027.2018.1551631 (2019).
Schneider, B. A., Daneman, M. & Murphy, D. R. Speech comprehension difficulties in older adults: Cognitive slowing or age-related changes in hearing? Psychol. Aging 20, 261–271 (2005).
pubmed: 16029090
doi: 10.1037/0882-7974.20.2.261
Deng, Y., Reinhart, R. M. & Choi, I. & Shinn-Cunningham, B. G. Causal links between parietal alpha activity and spatial auditory attention. Elife 8 (2019).
Baltzell, L. S., Swaminathan, J., Cho, A. Y., Lavandier, M. & Best, V. Binaural sensitivity and release from speech-on-speech masking in listeners with and without hearing loss. J. Acoust. Soc. Am. 147, 1546–1561 (2020).
pubmed: 32237845
pmcid: 7060089
doi: 10.1121/10.0000812
Heinrich, A., Henshaw, H. & Ferguson, M. A. The relationship of speech intelligibility with hearing sensitivity, cognition, and perceived hearing difficulties varies for different speech perception tests. Front. Psychol. 6, 1–14 (2015).
doi: 10.3389/fpsyg.2015.00782
British Society of Audiology. Recommended procedure: Pure tone air and bone conduction threshold audiometry with and without masking and determination of uncomfortable loudness levels. http://www.thebsa.org.uk/docs/bsapta.doc (2004).
Brainard, D. H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).
pubmed: 9176952
doi: 10.1163/156856897X00357
Moore, T. J. Voice communication jamming research. In AGARD Conference Proceedings 331: Aural Communication in Aviation 2:1–2:6 (1981).
Team J. JASP (Version 0.17.2.1) (2023).
Team J. JASP (Version 0.18.1.0) (2023).
Buchanan, E. M., Padfield, W. E., Van Nuland, A., Wikowsky, A. & Gillenwaters A. MOTE: The shiny app to calculate effect sizes and their confidence intervals (2018).
Lubczyk, T., Lukács, G. & Ansorge, U. Speed versus accuracy instructions in the response time concealed information test. Cogn. Res. Princ. Implic. 7, 1–11 (2022).
Vandierendonck, A. A comparison of methods to combine speed and accuracy measures of performance: A rejoinder on the binning procedure. Behav. Res. Methods 49, 653–673 (2017).
pubmed: 26944576
doi: 10.3758/s13428-016-0721-5