The effect of mild-to-moderate hearing loss on auditory and emotion processing networks

Frontiers in Systems Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Husain, Fatima T ^a   Carpenter Thompson, Jake R ^a   Schmidt, Sara A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Emotion; fMRI; Functional connectivity; Hearing loss; IADS; Resting state fMRI

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; AUDIOMETRY; BEHAVIORAL SCIENCE; CLINICAL ARTICLE; CONTROLLED STUDY; DORSAL ATTENTION NETWORK; EMOTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING IMPAIRMENT; HUMAN; INSULA; MALE; MIDDLE TEMPORAL GYRUS; PARAHIPPOCAMPAL GYRUS; PERCEPTION DEAFNESS; PRIMARY MOTOR CORTEX; PURE TONE AUDIOMETRY; REST;

EID: 84893581930     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00010     Document Type: Article

References (61)

1. Amaral, D. G., and Price, J. L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230, 465-496. doi: 10.1002/cne.902300402
2. Anticevic, A., Repovs, G., and Barch, D. M. (2012). Emotion effects on attention, amygdala activation, and functional connectivity in schizophrenia. Schizophr. Bull. 38, 967-980. doi: 10.1093/schbul/sbq168
3. Bartels, H., Middel, B. L., Van Der Laan, B. F., Staal, M. J., and Albers, F. W. (2008). The additive effect of co-occurring anxiety and depression on health status, quality of life and coping strategies in help-seeking tinnitus sufferers. Ear Hear. 29, 947-956. doi: 10.1097/AUD.0b013e3181888f83
4. Beck, A. T., and Steer, R. A. (1984). Internal consistencies of the original and revised Beck Depression Inventory. J. Clin. Psychol. 40, 1365-1367. doi: 10.1002/1097-4679(198411)40:6<1365::AID-JCLP2270400615>3.0.CO;2-D
5. Blood, A. J., and Zatorre, R. J. (2001). Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl. Acad. Sci. U.S.A. 98, 11818-11823. doi: 10.1073/pnas.191355898
6. Bradley, M. M., and Lang, P. J. (2007). The International Affective Digitized Sounds (IADS-2): Affective Ratings of Sounds and Instruction Manual. Gainesville, FL: University of Florida, Technical Report: B-3.
7. Brett, M., Anton, J. L., Valabregue, R., and Poline, J. B. (2002). Region of interest analysis using an SPM toolbox. NeuroImage 16, 1140-1141.
8. Burton, H., Wineland, A., Bhattacharya, M., Nicklaus, J., Garcia, K. S., and Piccirillo, J. F. (2012). Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci. 13:3. doi: 10.1186/1471-2202-13-3
9. Carabellese, C., Appollonio, I., Rozzini, R., Bianchetti, A., Frisoni, G. B., Frattola, L., et al. (1993). Sensory impairment and quality of life in a community elderly population. J. Am. Geriatr. Soc. 41, 401-407.
10. Cruickshanks, K. J., Wiley, T. L., Tweed, T. S., Klein, B. E., Klein, R., Mares-Perlman, J. A., et al. (1998). Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study. Am. J. Epidemiol. 148, 879-886. doi: 10.1093/oxfordjournals.aje.a009713
11. Davis, A., and Rafaie, E. A. (2000). "Epidemiology of tinnitus, " in Tinnitus Handbook, ed R. S. Tyler (San Diego, CA: Singular), 1-24.
12. Dolcos, F., and McCarthy, G. (2006). Brain systems mediating cognitive interference by emotional distraction. J. Neurosci. 26, 2072-2079. doi: 10.1523/JNEUROSCI.5042-05.2006
13. Feldmann, H., and Kumpf, W. (1988). [Listening to music in hearing loss with and without a hearing aid]. Laryngol. Rhinol. Otol. (Stuttg). 67, 489-497. doi: 10.1055/s-2007-998547
14. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673-9678. doi: 10.1073/pnas.0504136102
15. Franks, J. R. (1982). Judgments of hearing aid processed music. Ear Hear. 3, 18-23. doi: 10.1097/00003446-198201000-00004
16. Friston, K. J. (1994). Functional and effective connectivity in neuroimaging: a synthesis. Hum. Brain Mapp. 2, 56-78. doi: 10.1002/hbm.460020107
17. Gaab, N., Gaser, C., Zaehle, T., Jancke, L., and Schlaug, G. (2003). Functional anatomy of pitch memory-an fMRI study with sparse temporal sampling. Neuroimage 19, 1417-1426. doi: 10.1016/S1053-8119(03)00224-6
18. Giraud, A. L., Chery-Croze, S., Fischer, G., Fischer, C., Vighetto, A., Gregoire, M. C., et al. (1999). A selective imaging of tinnitus. Neuroreport 10, 1-5. doi: 10.1097/00001756-199901180-00001
19. Golm, D., Schmidt-Samoa, C., Dechent, P., and Kroner-Herwig, B. (2013). Neural correlates of tinnitus related distress: an fMRI-study. Hear. Res. 295, 87-99. doi: 10.1016/j.heares.2012.03.003
20. Gopinath, B., Wang, J. J., Schneider, J., Burlutsky, G., Snowdon, J., McMahon, C. M., et al. (2009). Depressive symptoms in older adults with hearing impairments: the Blue Mountains Study. J. Am. Geriatr. Soc. 57, 1306-1308. doi: 10.1111/j.1532-5415.2009.02317.x
21. Greicius, M. (2008). Resting-state functional connectivity in neuropsychiatric disorders. Curr. Opin. Neurol. 21, 424-430. doi: 10.1097/WCO.0b013e328306f2c5
22. Hall, D. A., Haggard, M. P., Akeroyd, M. A., Palmer, A. R., Summerfield, A. Q., Elliott, M. R., et al. (1999). "Sparse" temporal sampling in auditory fMRI. Hum. Brain Mapp. 7, 213-223. doi: 10.1002/(SICI)1097-0193(1999)7:3<213::AID-HBM5>3.0.CO;2-N
23. Hicks, C. B., and Tharpe, A. M. (2002). Listening effort and fatigue in school-age children with and without hearing loss. J. Speech Lang. Hear. Res. 45, 573. doi: 10.1044/1092-4388(2002/046)
24. Horwitz, B. (2003). The elusive concept of brain connectivity. Neuroimage 19, 466-470. doi: 10.1016/S1053-8119(03)00112-5
25. Husain, F. T., Medina, R. E., Davis, C. W., Szymko-Bennett, Y., Simonyan, K., Pajor, N. M., et al. (2011a). Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res. 1369, 74-88. doi: 10.1016/j.brainres.2010.10.095
26. Husain, F. T., Pajor, N. M., Smith, J. F., Kim, H. J., Rudy, S., Zalewski, C., et al. (2011b). Discrimination task reveals differences in neural bases of tinnitus and hearing impairment. PLoS ONE 6:e26639. doi: 10.1371/journal.pone.0026639
27. Husain, F. T., Patkin, D. J., Thai-Van, H., Braun, A. R., and Horwitz, B. (2009). Distinguishing the processing of gestures from signs in deaf individuals: An fMRI study. Brain Res. 1276, 140-150. doi: 10.1016/j.brainres.2009.04.034
28. Husain, F. T., and Schmidt, S. A. (2013). Using resting state functional connectivity to unravel networks of tinnitus. Hear. Res. 307, 154-162. doi: 10.1016/j.heares.2013.07.010
29. Jastreboff, P. J. (1990). Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci. Res. 8, 221-254. doi: 10.1016/0168-0102(90)90031-9
30. Koelsch, S., Fritz, T., Dy, V. C., Muller, K., and Friederici, A. D. (2006). Investigating emotion with music: an fMRI study. Hum. Brain Mapp. 27, 239-250. doi: 10.1002/hbm.20180
31. Kumar, S., Von Kriegstein, K., Friston, K., and Griffiths, T. D. (2012). Features versus feelings: dissociable representations of the acoustic features and valence of aversive sounds. J. Neurosci. 32, 14184-14192. doi: 10.1523/JNEUROSCI.1759-12.2012
32. Kundu, P., Brenowitz, N. D., Voon, V., Worbe, Y., Vertes, P. E., Inati, S. J., et al. (2013). Integrated strategy for improving functional connectivity mapping using multiecho fMRI. Proc. Natl. Acad. Sci. U.S.A. 110, 16187-16192. doi: 10.1073/pnas.1301725110
33. Kundu, P., Inati, S. J., Evans, J. W., Luh, W. M., and Bandettini, P. A. (2012). Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI. Neuroimage 60, 1759-1770. doi: 10.1016/j.neuroimage.2011.12.028
34. Leek, M. R., Molis, M. R., Kubli, L. R., and Tufts, J. B. (2008). Enjoyment of music by elderly hearing-impaired listeners. J. Am. Acad. Audiol. 19, 519-526. doi: 10.3766/jaaa.19.6.7
35. Li, Y., Booth, J. R., Peng, D., Zang, Y., Li, J., Yan, C., et al. (2013). Altered intra-and inter-regional synchronization of superior temporal cortex in deaf people. Cereb. Cortex 23, 1988-1996. doi: 10.1093/cercor/bhs185
36. Mather, M., and Knight, M. (2005). Goal-directed memory: the role of cognitive control in older adults' emotional memory. Psychol. Aging 20, 554-570. doi: 10.1037/0882-7974.20.4.554
37. Mirz, F., Gjedde, A., Ishizu, K., and Pedersen, C. B. (2000). Cortical networks subserving the perception of tinnitus-a PET study. Acta Otolaryngol. Suppl. 543, 241-243. doi: 10.1080/000164800454503
38. Mulrow, C. D., Aguilar, C., Endicott, J. E., Velez, R., Tuley, M. R., Charlip, W. S., et al. (1990). Association between hearing impairment and the quality of life of elderly individuals. J. Am. Geriatr. Soc. 38, 45-50.
39. Onoda, K., Ishihara, M., and Yamaguchi, S. (2012). Decreased functional connectivity by aging is associated with cognitive decline. J. Cogn. Neurosci. 24, 2186-2198. doi: 10.1162/jocn_a_00269
40. Peelle, J. E., Troiani, V., Grossman, M., and Wingfield, A. (2011). Hearing loss in older adults affects neural systems supporting speech comprehension. J. Neurosci. 31, 12638-12643. doi: 10.1523/JNEUROSCI.2559-11.2011
41. Petitto, L. A., Zatorre, R. J., Gauna, K., Nikelski, E. J., Dostie, D., and Evans, A. C. (2000). Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. Proc. Natl. Acad. Sci. U.S.A. 97, 13961-13966. doi: 10.1073/pnas.97.25.13961
42. Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320-341. doi: 10.1016/j.neuroimage.2013.08.048
43. Raichle, M. E., Macleod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682. doi: 10.1073/pnas.98.2.676
44. Rauschecker, J. P., Leaver, A. M., and Muhlau, M. (2010). Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66, 819-826. doi: 10.1016/j.neuron.2010.04.032
45. Rutledge, K. L. (2009). A Music Listening Questionnaire for Hearing Aid Users. Unpublished Master's Thesis. University of Canterbury, Christchurch. Available online at: http://hdl.handle.net/10092/3194
46. Schmidt, S. A., Akrofi, K., Carpenter-Thompson, J. R., and Husain, F. T. (2013). Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. PLoS ONE 8:e76488. doi: 10.1371/journal.pone.0076488
47. Seydell-Greenwald, A., Leaver, A. M., Turesky, T. K., Morgan, S., Kim, H. J., and Rauschecker, J. P. (2012). Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus. Brain Res. 1485, 22-39. doi: 10.1016/j.brainres.2012.08.052
48. Steer, R. A., Clark, D. A., Beck, A. T., and Ranieri, W. F. (1999). Common and specific dimensions of self-reported anxiety and depression: the BDI-II versus the BDI-IA. Behav. Res. Ther. 37, 183-190. doi: 10.1016/S0005-7967(98)00087-4
49. Steer, R. A., Ranieri, W. F., Beck, A. T., and Clark, D. A. (1993). Further evidence for the validity of the Beck Anxiety Inventory with psychiatric outpatients. J. Anxiety Disord. 7, 195-205. doi: 10.1016/0887-6185(93)90002-3
50. Stevens, G., Flaxman, S., Brunskill, E., Mascarenhas, M., Mathers, C. D., Finucane, M., et al. (2013). Global and regional hearing impairment prevalence: an analysis of 42 studies in 29 countries. Eur. J. Public Health 23, 146-152. doi: 10.1093/eurpub/ckr176
51. St Jacques, P., Dolcos, F., and Cabeza, R. (2010). Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data. Neurobiol. Aging 31, 315-327. doi: 10.1016/j.neurobiolaging.2008.03.012
52. Tschacher, W., Schildt, M., and Sander, K. (2010). Brain connectivity in listening to affective stimuli: a functional magnetic resonance imaging (fMRI) study and implications for psychotherapy. Psychother. Res. 20, 576-588. doi: 10.1080/10503307.2010.493538
53. Tun, P. A., McCoy, S., and Wingfield, A. (2009). Aging, hearing acuity, and the attentional costs of effortful listening. Psychol. Aging 24, 761-766. doi: 10.1037/a0014802
54. Uys, M., Pottas, L., Vinck, B., and Van Dijk, C. (2012). The influence of non-linear frequency compression on the perception of music by adults with a moderate to sever hearing loss: subjective impressions. S. Afr. J. Commun. Disord. 59, 53-67. doi: 10.7196/sajcd.119
55. Van Dijk, K. R., Sabuncu, M. R., and Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431-438. doi: 10.1016/j.neuroimage.2011.07.044
56. Weisz, N., Voss, S., Berg, P., and Elbert, T. (2004). Abnormal auditory mismatch response in tinnitus sufferers with high-frequency hearing loss is associated with subjective distress level. BMC Neurosci. 5:8. doi: 10.1186/1471-2202-5-8
57. Whitfield-Gabrieli, S., and Nieto-Castanon, A. (2012). Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2, 125-141. doi: 10.1089/brain.2012.0073
58. Wong, P. C., Ettlinger, M., Sheppard, J. P., Gunasekera, G. M., and Dhar, S. (2010). Neuroanatomical characteristics and speech perception in noise in older adults. Ear Hear. 31, 471-479. doi: 10.1097/AUD.0b013e3181d709c2
59. Yoneda, M., Ikawa, M., Arakawa, K., Kudo, T., Kimura, H., Fujibayashi, Y., et al. (2012). In vivo functional brain imaging and a therapeutic trial of L-arginine in MELAS patients. Biochim. Biophys. Acta 1820, 615-618. doi: 10.1016/j.bbagen.2011.04.018
60. Yueh, B., Shapiro, N., Maclean, C. H., and Shekelle, P. G. (2003). Screening and management of adult hearing loss in primary care: scientific review. JAMA 289, 1976-1985. doi: 10.1001/jama.289.15.1976
61. Zaehle, T., Wustenberg, T., Meyer, M., and Jancke, L. (2004). Evidence for rapid auditory perception as the foundation of speech processing: a sparse temporal sampling fMRI study. Eur. J. Neurosci. 20, 2447-2456. doi: 10.1111/j.1460-9568.2004.03687.x