Journal of Biomedical Engineering Research (대한의용생체공학회:의공학회지)

The Korean Society of Medical and Biological Engineering (대한의용생체공학회)
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Neural Correlates of Language Processing in Adults with Hearing Loss and Normal Hearing: An fNIRS Study Using Verbal Fluency and Discourse Tasks

fNIRS를 통한 언어 유창성 및 담화 과제 수행 중 난청 및 건청 성인의 신경 처리 특성 비교

  • Su Been Kim (Department of Communication Disorders, Ewha Womans University) ;
  • Jaeyoung Shin (Department of AI Data Engineering, Korea National University of Transportation) ;
  • Hye Yoon Seol (Department of Communication Disorders, Ewha Womans University)
  • 김수빈 (이화여자대학교 언어병리학과) ;
  • 신재영 (국립한국교통대학교 AI데이터공학부) ;
  • 설혜윤 (이화여자대학교 언어병리학과)
  • Received : 2025.12.19
  • Accepted : 2026.02.11
  • Published : 2026.02.28
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Abstract

This study aimed to investigate the impact of hearing loss (HL) on language processing abilities and brain activation patterns in adults with HL and normal hearing (NH) using functional near-infrared spectroscopy (fNIRS). Hemodynamic responses in the prefrontal cortex were measured using fNIRS while participants performed phonemic and semantic verbal fluency tasks and a discourse task. Behavioral performance was analyzed in conjunction with fNIRS data to examine group differences in task performance and associated neural effort. The HL group exhibited significantly lower performance on the phonemic fluency task compared to the NH group, accompanied by greater prefrontal activation. This suggests increased cognitive load and the recruitment of additional cognitive resources during phonological processing in individuals with HL. Although group differences in performance on the semantic fluency task were less pronounced, significant differences in deoxyhemoglobin levels were observed, indicating altered neural processing associated with HL. This pattern suggests compensatory neural mechanisms involving functional reorganization and redistribution of cognitive resources. In the discourse task, the HL group showed reduced performance; however, no significant group differences in prefrontal activation were found, implying comparable levels of cognitive effort but reduced processing efficiency in the HL group. The findings show the importance of sustained and adequate auditory experience not only for speech perception, vocabulary development, and articulation but also for mitigating increased cognitive load in individuals with HL. These results provide baseline data to support the development of personalized rehabilitation strategies and educational approaches in communication disorders, highlighting the clinical relevance of investigating the central effects of HL.

Keywords

Acknowledgement

This work was supported by the Ministry of Education of the Republic of Korea and the National Research Foundation of Korea(NRF-2023S1A5A2A03085474).

References

  1. Briscoe J, Bishop DV, Norbury CF. Phonological processing, language, and literacy: a comparison of children with mildto-moderate sensorineural hearing loss and those with specific language impairment. J Child Psychol Psychiatry. 2001;42(3): 329-40. https://doi.org/10.1111/jcpp.2001.42.issue-3
  2. Chapman RS. Children's language learning: an interactionist perspective. J Child Psychol Psychiatry. 2000;41(1):33-54. https://doi.org/10.1111/jcpp.2000.41.issue-1
  3. Tomblin JB, Harrison M, Ambrose SE, Walker EA, Oleson JJ, Moeller MP. Language outcomes in young children with mild to severe hearing loss. Ear Hear. 2015;36:76S-91S. https://doi.org/10.1097/AUD.0000000000000219
  4. Davis JM, Elfenbein J, Schum R, Bentler RA. Effects of mild and moderate hearing impairments on language, educational, and psychosocial behavior of children. J Speech Hear Disord. 1986;51(1):53-62. https://doi.org/10.1044/jshd.5101.53
  5. Moradi S, Lidestam B, Hällgren M, Rönnberg J. Gated auditory speech perception in elderly hearing aid users and elderly normal-hearing individuals: Effects of hearing impairment and cognitive capacity. Trends Hear. 2014;18:2331216514545406. https://doi.org/10.1177/2331216514545406
  6. Classon E, Löfkvist U, Rudner M, Rönnberg J. Verbal fluency in adults with postlingually acquired hearing impairment. Speech Lang Hear. 2014;17(2):88-100. https://doi.org/10.1179/205057113X13781290153457
  7. Santos IMMD, Chiossi JSC, Soares AD, Oliveira LND, Chiari BM. Phonological and semantic verbal fluency: a comparative study in hearing-impaired and normal-hearing people. CoDAS. 2014;26(4):273-8.
  8. Chandrashekar P, Nagaraj H. Verbal Fluency as a Measure of Executive Function in Middle-Aged Adults with Mild Sensorineural Hearing Loss. Indian J Otolaryngol Head Neck Surg. 2024;76(6):5443-50. https://doi.org/10.1007/s12070-024-04999-9
  9. Soares AD, Goulart BNG, Chiari BM. Narrative competence among hearing-impaired and normal-hearing children: analytical cross-sectional study. Sao Paulo Med J. 2010;128(5):284-8. https://doi.org/10.1590/S1516-31802010000500008
  10. Arfé B, Rossi C, Sicoli S. The contribution of verbal working memory to deaf children's oral and written production. J Deaf Stud Deaf Educ. 2015;20(3):203-14. https://doi.org/10.1093/deafed/env005
  11. Lee Y, Yim D, Sim H. Phonological processing skills and its relevance to receptive vocabulary development in children with early cochlear implantation. Int J Pediatr Otorhinolaryngol. 2012;76(12):1755-60. https://doi.org/10.1016/j.ijporl.2012.08.016
  12. de Hoog BE, Langereis MC, van Weerdenburg M, Knoors H, Verhoeven L. Lexical access in children with hearing loss or specific language impairment, using the cross-modal picture–word interference paradigm. Res Dev Disabil. 2015;37:81-94. https://doi.org/10.1016/j.ridd.2014.11.007
  13. Klein KE, Walker EA, McMurray B. Delayed lexical access and cascading effects on spreading semantic activation during spoken word recognition in children with hearing aids and cochlear implants: Evidence from eye-tracking. Ear Hear. 2023;44(2):338-57. https://doi.org/10.1097/AUD.0000000000001286
  14. Glick HA, Sharma A. Cortical neuroplasticity and cognitive function in early-stage, mild-moderate hearing loss: evidence of neurocognitive benefit from hearing aid use. Front Neurosci. 2020;14:93. https://doi.org/10.3389/fnins.2020.00093
  15. Madashetty S, Palaniswamy HP, Rajashekhar B. Investigating the impact of hearing loss on attentional networks among older individuals: an event-related potential study. Cogn Neurodyn. 2024;18(5):3093-105.
  16. Habicht J, Behler O, Kollmeier B, Neher T. Exploring differences in speech processing among older hearing-impaired listeners with or without hearing aid experience: Eye-tracking and fMRI measurements. Front Neurosci. 2019;13:420. https://doi.org/10.3389/fnins.2019.00420
  17. Moteki H, Suzuki M, Naito Y, Fujiwara K, Oguchi K, Nishio SY, Iwasaki S, Usami SI. Evaluation of cortical processing of language by use of positron emission tomography in hearing loss children with congenital cytomegalovirus infection. Int J Pediatr Otorhinolaryngol. 2014;78(2):285-289. https://doi.org/10.1016/j.ijporl.2013.11.025
  18. Li Q, Xia S, Zhao f, Qi J. Functional changes in people with different hearing status and experiences of using Chinese sign language: an fMRI study. J Commun Disord. 2014;50:51-60. https://doi.org/10.1016/j.jcomdis.2014.05.001
  19. Seol HY, Shin J. A review of the Implementation of Functional Brain Imaging Techniques in Auditory Research focusing on Hearing Loss. J Biomed Eng Res. 2024;45(1):26-36.
  20. Herrmann MJ, Horst AK, Löble S, Möll MT, Katzorke A, Polak T. Relevance of dorsolateral and frontotemporal cortex on the phonemic verbal fluency–a fNIRS-study. Neuroscience. 2017;367:169-77. https://doi.org/10.1016/j.neuroscience.2017.10.028
  21. Hatta T, Kanari A, Mase M, Kabasawa H, Ogawa T, Shirataki T, Hibino S, Iwahara A, Fujiwara K, Hamajima N. Brain Mechanisms in Japanese Verbal Fluency Test: Evidence from Examination by NIRS (Near-Infrared Spectroscopy). Asia Pac J Speech Lang Hear. 2008;11(2):103-110. https://doi.org/10.1179/136132808805297250
  22. Bisconti S, Shulkin M, Hu X, Basura GJ, Kileny PR, Kovelman I. Functional near-infrared spectroscopy brain imaging investigation of phonological awareness and passage comprehension abilities in adult recipients of cochlear implants. J Speech Lang Hear Res. 2016;59(2):239-53. https://doi.org/10.1044/2015_JSLHR-L-14-0278
  23. Olds C, Pollonini L, Abaya H, Larky J, Loy M, Bortfeld H, Beauchamp MS, Oghalai JS. Cortical activation patterns correlate with speech understanding after cochlear implantation. Ear Hear. 2016;37(3):e160-72. https://doi.org/10.1097/AUD.0000000000000258
  24. Van de Rijt LP, Van Opstal AJ, Mylanus EA, Straatman LV, Hu HY, Snik AF, Van Wanrooij MM. Temporal cortex activation to audiovisual speech in normal-hearing and cochlear implant users measured with functional near-infrared spectroscopy. Front Hum Neurosci. 2016;10:48. https://doi.org/10.3389/fnhum.2016.00048
  25. Campbell J, Sharma A. Cross-modal re-organization in adults with early stage hearing loss. PLoS One. 2014;9(2):e90594. https://doi.org/10.1371/journal.pone.0090594
  26. Bortfeld H. Functional near‐infrared spectroscopy as a tool for assessing speech and spoken language processing in pediatric and adult cochlear implant users. Dev Psychobiol. 2019;61(3):430-43. https://doi.org/10.1002/dev.v61.3
  27. Farrar R, Ashjaei S, Arjmandi MK. Speech-evoked cortical activities and speech recognition in adult cochlear implant listeners: a review of functional near-infrared spectroscopy studies. Exp Brain Res. 2024;242(11):2509-30.
  28. Barrot JS. Comparing the linguistic complexity in receptive and productive modes. GEMA Online J Lang Stud. 2015; 15(2):65-81. https://doi.org/10.17576/gema
  29. Gibson TA, Peña ED, Bedore LM. The relation between language experience and receptive-expressive semantic gaps in bilingual children. Int J Bil Educ Bil. 2014;17(1):90-110. https://doi.org/10.1080/13670050.2012.743960
  30. Sook LM, Kim BS. Characteristics of Word Fluency in Healthy Aging and Alzheimer's Disease. Audiol Speech Res. 2019; 15(2):135-43. https://doi.org/10.21848/asr.2019.15.2.135
  31. Kang Y, Na DL. Seoul Neuropsychological Screening Battery. Human Brain Research & Consulting; 2003.
  32. Kang Y, Chin JH, Na DL, Lee J, Park JS. A normative study of the Korean version of Controlled Oral Word Association Test (COWAT) in the elderly. Korean J Clin Psychol. 2000; 19(2):385-92.
  33. Cannizzaro MS, Stephens SR, Michael SC, Shaun RS. Discourse formulation and neurovascular activation across four genres. Clin Arch Commun Disord. 2019;4(1):10-20. https://doi.org/10.21849/cacd.
  34. Kim HH, Lee HJ, Kim DY, Heo JH, Kim YW. A Preliminary Study for Development of the Aphasia Screening Test. Speech Sci. 2006;13(2):7-18.
  35. Kim BS. The Preliminary Study on the Development of the Brief Test of Cognitive-Communication Disorders: Correlation between Discourse Performance and Cognitive Functions by Age. J Spec Educ Rehabil Sci. 2020;59(4):331-52.
  36. León-Carrión J, León-Domínguez U. Functional near-infrared spectroscopy (fNIRS): principles and neuroscientific applications. Neuroimaging. 2012;97:48-74.
  37. Kocsis L, Herman P, Eke A. The modified Beer–Lambert law revisited. Phys Med Biol. 2006;51(5):N91. https://doi.org/10.1088/0031-9155/51/5/N02
  38. Yücel MA, Huppert TJ, Boas DA, Gagnon L. Calibrating the BOLD signal during a motor task using an extended fusion model incorporating DOT, BOLD and ASL data. NeuroImage. 2012;61(4):1268-76. https://doi.org/10.1016/j.neuroimage.2012.04.036
  39. Luke R, Larson E, Shader MJ, Innes-Brown H, Van Yper L, Lee AKC, Sowman PF, McAlpine D. Analysis methods for measuring passive auditory fNIRS responses generated by a block-design paradigm. Neurophotonics. 2021;8(2):025008. https://doi.org/10.1117/1.NPh.8.2.025008
  40. Yaramothu C, Li X, Morales C, Alvarez TL. Reliability of frontal eye fields activation and very low-frequency oscillations observed during vergence eye movements: an fNIRS study. Sci Rep. 2020;10(1):712. https://doi.org/10.1038/s41598-020-57597-4
  41. Cohen J. Statistical power analysis for the behavioral sciences. Routledge; 2013.
  42. Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol. 2013;4:863. https://doi.org/10.3389/fpsyg.2013.00863
  43. Rende B, Ramsberger G, Miyake A. Commonalities and differences in the working memory components underlying letter and category fluency tasks: a dual-task investigation. Neuropsychology. 2002;16(3):309-16. https://doi.org/10.1037/0894-4105.16.3.309
  44. Montgomery JW, Evans JL, Gillam RB. Relation of auditory attention and complex sentence comprehension in children with specific language impairment: A preliminary study. Appl Psycholinguist. 2009;30(1):123-51. https://doi.org/10.1017/S0142716408090061
  45. Lund E. Vocabulary knowledge of children with cochlear implants: A meta-analysis. J Deaf Stud Deaf Educ. 2016;21(2): 107-21. https://doi.org/10.1093/deafed/env060
  46. Majorano M, Brondino M, Morelli M, Ferrari R, Lavelli M, Guerzoni L, Cuda D, Persici V. Preverbal Production and Early Lexical Development in Children With Cochlear Implants: A Longitudinal Study Following Pre-implanted Children Until 12 Months After Cochlear Implant Activation. Front Psychol. 2020;11:591584. https://doi.org/10.3389/fpsyg.2020.591584
  47. Busch T, Brinchmann EI, Braeken J, Wie OB. Receptive vocabulary of children with bilateral cochlear implants from 3 to 16 years of age. Ear Hear. 2022;43(6):1866-80. https://doi.org/10.1097/AUD.0000000000001220
  48. Werfel KL, Reynolds G, Hudgins S, Castaldo M, Lund EA. The production of complex syntax in spontaneous language by 4-year-old children with hearing loss. Am J Speech Lang Pathol. 2021;30(2):609-21. https://doi.org/10.1044/2020_AJSLP-20-00178
  49. Azuma T. Working memory and perseveration in verbal fluency. Neuropsychology. 2004;18(1):69-77. https://doi.org/10.1037/0894-4105.18.1.69
  50. Marshall CR, Jones A, Fastelli A, Atkinson J, Botting N, Morgan G. Semantic fluency in deaf children who use spoken and signed language in comparison with hearing peers. Int J Lang Commun Disord. 2018;53(1):157-70. https://doi.org/10.1111/1460-6984.2018.53.issue-1
  51. Kramer S, Vasil KJ, Adunka OF, Pisoni DB, Moberly AC. Cognitive functions in adult cochlear implant users, cochlear implant candidates, and normal-hearing listeners. Laryngoscope Investig Otolaryngol. 2018;3(4):304-10. https://doi.org/10.1002/lio2.v3.4
  52. Zhan KY, Lewis JH, Vasil KJ, Tamati TN, Harris MS, Pisoni DB, Kronenberger WG, Ray C, Moberly AC. Cognitive Functions in Adults Receiving Cochlear Implants: Predictors of Speech Recognition and Changes After Implantation. Otol Neurotol. 2020;41(3):e322-e329. https://doi.org/10.1097/MAO.0000000000002544
  53. Baldo JV, Schwartz S, Wilkins D, Dronkers NF. Role of frontal versus temporal cortex in verbal fluency as revealed by voxelbased lesion symptom mapping. J Int Neuropsychol Soc. 2006;12(6):896-900. https://doi.org/10.1017/S1355617706061078
  54. Gourovitch ML, Kirkby BS, Goldberg TE, Weinberger DR, Gold JM, Esposito G, Van Horn JD, Berman KF. A comparison of rCBF patterns during letter and semantic fluency. Neuropsychology. 2000;14(3):353-360. https://doi.org/10.1037/0894-4105.14.3.353
  55. Costafreda SG, Fu CH, Lee L, Everitt B, Brammer MJ, David AS. A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum Brain Mapp. 2006;27(10):799-810. https://doi.org/10.1002/hbm.v27:10
  56. Troyer AK, Moscovitch M, Winocur G. Clustering and switching as two components of verbal fluency: evidence from younger and older healthy adults. Neuropsychology. 1997;11(1):138-46. https://doi.org/10.1037/0894-4105.11.1.138
  57. Troyer AK, Moscovitch M, Winocur G, Alexander MP, Stuss DO. Clustering and switching on verbal fluency: The effects of focal frontal-and temporal-lobe lesions. Neuropsychologia. 1998;36(6):499-504. https://doi.org/10.1016/S0028-3932(97)00152-8
  58. Wen J, Yu T, Liu L, Hu Z, Yan J, Li Y, Li X. Evaluating the roles of left middle frontal gyrus in word production using electrocorticography. Neurocase. 2017;23(5-6):263-269. https://doi.org/10.1080/13554794.2017.1387275
  59. Sherafati A, Dwyer N, Bajracharya A, Hassanpour MS, Eggebrecht AT, Firszt JB, Culver JP, Peelle JE. Prefrontal cortex supports speech perception in listeners with cochlear implants. eLife. 2022;11:e75323. https://doi.org/10.7554/eLife.75323
  60. Chen Y, Wang S, Yang L, Liu Y, Fu X, Wang Y, Zhang X, Wang S. Features of the speech processing network in post- and prelingually deaf cochlear implant users. Cereb Cortex. 2024; 34(1):bhad417. https://doi.org/10.1093/cercor/bhad417
  61. Yoshida H, Takahashi H, Kanda Y, Chiba K. PET-CT observations of cortical activity in pre-lingually deaf adolescent and adult patients with cochlear implantation. Acta Otolaryngol. 2017;137(5):464-70. https://doi.org/10.1080/00016489.2016.1253868
  62. Strangman G, Culver JP, Thompson JH, Boas DA. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage. 2002;17(2):719-31. https://doi.org/10.1006/nimg.2002.1227
  63. Huppert TJ, Hoge RD, Diamond SG, Franceschini MA, Boas DA. A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage. 2006;29(2):368-82. https://doi.org/10.1016/j.neuroimage.2005.08.065
  64. Yeung MK. Frontal cortical activation during emotional and non-emotional verbal fluency tests. Sci Rep. 2022;12(1):8497. https://doi.org/10.1038/s41598-022-12559-w
  65. Lin FR, Ferrucci L, An Y, Goh JO, Doshi J, Metter EJ, Davatzikos C, Kraut MA, Resnick SM. Association of hearing impairment with brain volume changes in older adults. Neuroimage. 2014;90:84-92. https://doi.org/10.1016/j.neuroimage.2013.12.059
  66. Jones DT, Graff-Radford J. Executive dysfunction and the prefrontal cortex. Continuum (Minneap Minn). 2021;27(6):1586-1601. https://doi.org/10.1212/CON.0000000000001009
  67. Xu J, Kemeny S, Park G, Frattali C, Braun A. Language in context: emergent features of word, sentence, and narrative comprehension. Neuroimage. 2005;25(3):1002-15. https://doi.org/10.1016/j.neuroimage.2004.12.013
  68. Dunst B, Benedek M, Jauk E, Bergner S, Koschutnig K, Sommer M, Ischebeck A, Spinath B, Arendasy M, Bühner M, Freudenthaler H, Neubauer AC. Neural efficiency as a function of task demands. Intelligence. 2014;42:22-30. https://doi.org/10.1016/j.intell.2013.09.005
  69. Cannizzaro MS, Dumas J, Prelock P, Newhouse P. Organizational structure reduces processing load in the prefrontal cortex during discourse processing of written text: Implications for high-level reading issues after TBI. Perspect Neurophysiol Neurogenic Speech Lang Disord. 2012;22(2):67-78. https://doi.org/10.1044/nnsld22.2.67
  70. Xu LC, Zhang G, Zou Y, Zhang MF, Zhang DS, Ma H, Zhao WB, Zhang GY. Abnormal neural activities of directional brain networks in patients with long-term bilateral hearing loss. Oncotarget. 2017;8(48):84168-84179. https://doi.org/10.18632/oncotarget.v8i48
  71. Corina DP, Lawyer LA, Hauser P, Hirshorn E. Lexical processing in deaf readers: An fMRI investigation of reading proficiency. PLoS One. 2013;8(1):e54696. https://doi.org/10.1371/journal.pone.0054696
  72. Mackenzie C. Adult spoken discourse: the influences of age and education. Int J Lang Commun Disord. 2000;35(2):269-91. https://doi.org/10.1080/136828200247188
  73. Shao Z, Janse E, Visser K, Meyer AS. What do verbal fluency tasks measure? Predictors of verbal fluency performance in older adults. Front Psychol. 2014;5:772. https://doi.org/10.3389/fpsyg.2014.00772