Advertisement

Brain Topography

, Volume 31, Issue 2, pp 270–287 | Cite as

Cortical Processing of Level Cues for Spatial Hearing is Impaired in Children with Prelingual Deafness Despite Early Bilateral Access to Sound

  • Vijayalakshmi Easwar
  • Hiroshi Yamazaki
  • Michael Deighton
  • Blake Papsin
  • Karen Gordon
Original Paper

Abstract

Bilateral cochlear implantation aims to restore binaural hearing, important for spatial hearing, to children who are deaf. Improvements over unilateral implant use are attributed largely to the detection of interaural level differences (ILDs) but emerging evidence of impaired sound localization and binaural fusion suggest that these binaural cues are abnormally coded by the auditory system. We used multichannel electroencephalography (EEG) to assess cortical responses to ILDs in two groups: 13 children who received early bilateral cochlear implants (CIs) simultaneously, known to protect the developing auditory cortices from unilaterally driven reorganization, and 15 age matched peers with normal hearing. EEG source analyses indicated a dominance of right auditory cortex in both groups. Expected reductions in activity to ipsilaterally weighted ILDs were evident in the right hemisphere of children with normal hearing. By contrast, cortical activity in children with CIs showed: (1) limited ILD sensitivity in either cortical hemisphere, (2) limited correlation with reliable behavioral right-left lateralization of ILDs (in 10/12 CI users), and (3) deficits in parieto-occipital areas and the cerebellum. Thus, expected cortical ILD coding develops with normal hearing but is affected by developmental deafness despite early and simultaneous bilateral implantation. Findings suggest that impoverished fidelity of ILDs in independently functioning CIs may be impeding development of cortical ILD sensitivity in children who are deaf but do not altogether limit benefits of listening with bilateral CIs. Future efforts to provide consistent/accurate ILDs through auditory prostheses including CIs could improve binaural hearing for children with hearing loss.

Keywords

Beamformer Binaural hearing Bilateral cochlear implant Electroencephalography 

Notes

Acknowledgements

Authors thank Melissa Polonenko for assisting with preliminary data collection and analysis of behavioral data, and Salima Jiwani, Daniel Wong and Carmen McKnight for response analysis.

Funding

This work was supported by Restracomp fellowship awarded to Vijayalakshmi Easwar and Canadian Institute for Health Research awarded to Karen Gordon.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interests.

References

  1. Aronoff JM, Yoon Y-S, Freed DJ et al (2010) The use of interaural time and level difference cues by bilateral cochlear implant users. J Acoust Soc Am 127:EL87–EL92CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aronoff JM, Freed DJ, Fisher LM et al (2012) Cochlear implant patients’ localization using interaural level differences exceeds that of untrained normal hearing listeners. J Acoust Soc Am 131:EL382–EL387CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ashmead DH, Davis DL, Whalen T, Odom RD (1991) Sound localization and sensitivity to interaural time differences in human infants. Child Dev 62:1211–1226CrossRefPubMedGoogle Scholar
  4. Baumann O, Mattingley JB (2010) Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci Methods 30:4489–4495CrossRefGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  6. Blair RC, Karniski W (1993) An alternative method for significance testing of waveform difference potentials. Psychophysiology 30:518–524CrossRefPubMedGoogle Scholar
  7. Blatchley BJ, Brugge JF (1990) Sensitivity to binaural intensity and phase difference cues in kitten inferior colliculus. J Neurophysiol 64:582–597CrossRefPubMedGoogle Scholar
  8. Brugge JF, Reale RA, Wilson GF (1988) Sensitivity of auditory cortical neurons of kittens to monaural and binaural high frequency sound. Hear Res 34:127–140CrossRefPubMedGoogle Scholar
  9. Brunetti M, Belardinelli P, Caulo M et al (2005) Human brain activation during passive listening to sounds from different locations: an fMRI and MEG study. Human Brain Mapp 26:251–261CrossRefGoogle Scholar
  10. Bundy RS (1980) Discrimination of sound localization cues in young infants. Child Dev 51:292–294CrossRefPubMedGoogle Scholar
  11. Bushara KO, Weeks RA, Ishii K et al (1999) Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat Neurosci 2:759–766CrossRefPubMedGoogle Scholar
  12. Campbell RAA, Schnupp JWH, Shial A, King AJ (2006) Binaural-level functions in ferret auditory cortex: evidence for a continuous distribution of response properties. J Neurophysiol 95:3742–3755CrossRefPubMedGoogle Scholar
  13. Cavanna AE, Trimble M (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583CrossRefPubMedGoogle Scholar
  14. Chau W, McIntosh AR, Robinson SE et al (2004) Improving permutation test power for group analysis of spatially filtered MEG data. Neuroimage 23:983–996CrossRefPubMedGoogle Scholar
  15. Collignon O, Davare M, De Volder AG et al (2008) Time-course of posterior parietal and occipital cortex contribution to sound localization. J Cogn Neurosci 20:1454–1463CrossRefPubMedGoogle Scholar
  16. Cone-Wesson B, Ma E, Fowler CG (1997) Effect of stimulus level and frequency on ABR and MLR binaural interaction in human neonates. Hear Res 106:163–178CrossRefPubMedGoogle Scholar
  17. Dalal SS, Sekihara K, Nagarajan SS (2006) Modified beamformers for coherent source region suppression. IEEE Trans Biomed Eng 53:1357–1363CrossRefPubMedPubMedCentralGoogle Scholar
  18. Di Nardo W, Ippolito S, Quaranta N et al (2003) Correlation between NRT measurement and behavioural levels in patients with the nucleus 24 cochlear implant. Acta Otorhinolaryngol Ital 23:352–355PubMedGoogle Scholar
  19. Ducommun CY, Murray MM, Thut G et al (2002) Segregated processing of auditory motion and auditory location: an ERP mapping study. Neuroimage 16:76–88CrossRefPubMedGoogle Scholar
  20. Easwar V, Sanfilippo J, Papsin BC, Gordon KA (2016) Factors affecting daily cochlear implant use inchildren: datalogging evidence. J Am Acad Audiol 27:824–838CrossRefPubMedGoogle Scholar
  21. Easwar V, Yamazaki H, Deighton M et al (2017a) Cortical representation of interaural time difference is impaired by deafness in development: evidence from children with early long-term access to sound through bilateral cochlear implants provided simultaneously. J Neurosci 37:2349–2361CrossRefPubMedGoogle Scholar
  22. Easwar V, Yamazaki H, Deighton M et al (2017b) Simultaneous bilateral cochlear implants: developmental advances do not yet achieve normal cortical processing. Brain Behav 20:e00638–e00615CrossRefGoogle Scholar
  23. Franklin SR, Brunso-Bechtold JK, Henkel CK (2008) Bilateral cochlear ablation in postnatal rat disrupts development of banded pattern of projections from the dorsal nucleus of the lateral lemniscus to the inferior colliculus. Neuroscience 154:346–354CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gordon KA, Papsin BC (2013) From nucleus 24 to 513: changing cochlear implant design affects auditory response thresholds. Otol Neurotol 34:436–442CrossRefPubMedGoogle Scholar
  25. Gordon KA, Papsin BC, Harrison RV (2007) Auditory brainstem activity and development evoked by apical versus basal cochlear implant electrode stimulation in children. Clin Neurophysiol 118:1671–1684CrossRefPubMedGoogle Scholar
  26. Gordon KA, Tanaka S, Wong DE et al (2011) Multiple effects of childhood deafness on cortical activity in children receiving bilateral cochlear implants simultaneously. Clin Neurophysiol 122:823–833CrossRefPubMedGoogle Scholar
  27. Gordon KA, Salloum C, Toor GS et al (2012) Binaural interactions develop in the auditory brainstem of children who are deaf: effects of place and level of bilateral electrical stimulation. J Neurosci 32:4212–4223CrossRefPubMedGoogle Scholar
  28. Gordon KA, Wong DE, Papsin BC (2013) Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf. Brain 136:1609–1625CrossRefPubMedGoogle Scholar
  29. Gordon KA, Deighton MR, Abbasalipour P, Papsin BC (2014) Perception of binaural cues develops in children who are deaf through bilateral cochlear implantation. PLoS ONE 9:e114841CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gordon KA, Henkin Y, Kral A (2015) Asymmetric hearing during development: the aural preference syndrome and treatment options. Pediatrics 136:141–153CrossRefPubMedGoogle Scholar
  31. Gordon KA, Abbasalipour P, Papsin BC (2016) Balancing current levels in children with bilateral cochlear implants using electrophysiological and behavioural measures. Hear Res 335:193–206CrossRefPubMedGoogle Scholar
  32. Grantham DW, Ashmead DH, Ricketts TA et al (2007) Horizontal-plane localization of noise and speech signals by postlingually deafened adults fitted with bilateral cochlear implants. Ear Hear 28:524–541CrossRefPubMedGoogle Scholar
  33. Grantham DW, Ashmead DH, Ricketts TA et al (2008) Interaural time and level difference thresholds for acoustically presented signals in post-lingually deafened adults fitted with bilateral cochlear implants using CIS+ processing. Ear Hear 29:33–44PubMedGoogle Scholar
  34. Griffiths TD, Rees G, Rees A et al (1998) Right parietal cortex is involved in the perception of sound movement in humans. Nat Neurosci 1:74–79CrossRefPubMedGoogle Scholar
  35. Grothe B, Pecka M (2014) The natural history of sound localization in mammals: a story of neuronal inhibition. Front Neural Circuits 8:1–19CrossRefGoogle Scholar
  36. Hancock KE, Noel V, Ryugo DKK, Delgutte B (2010) Neural coding of interaural time differences with bilateral cochlear implants: effects of congenital deafness. J Neurosci 30:14068–14079CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hartmann R, Topp G, Klinke R (1984) Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea. Hear Res 13:47–62CrossRefPubMedGoogle Scholar
  38. Jiwani S, Papsin BC, Gordon KA (2016) Early unilateral cochlear implantation promotes mature cortical asymmetries in adoloscents who are deaf. Human Brain Mapp 37:135–152CrossRefGoogle Scholar
  39. Johnson BW, Hautus MJ (2010) Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 48:2610–2619CrossRefPubMedGoogle Scholar
  40. Johnson BW, Hautus MJ, Duff DJ, Clapp WC (2007) Sequential processing of interaural timing differences for sound source segregation and spatial localization: evidence from event-related cortical potentials. Psychophysiology 44:541–551CrossRefPubMedGoogle Scholar
  41. Kaga M (1992) Development of sound localization. Acta Paediatr Jpn 34:134–138CrossRefPubMedGoogle Scholar
  42. Kan A, Litovsky RY (2015) Binaural hearing with electrical stimulation. Hear Res 322:127–137CrossRefPubMedGoogle Scholar
  43. Koch U, Sanes DH (1998) Afferent regulation of glycine receptor distribution in the gerbil LSO. Microsc Res Tech 41:263–269CrossRefPubMedGoogle Scholar
  44. Kotak VC, Sanes DH (1996) Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J Neurosci 16:1836–1843PubMedGoogle Scholar
  45. Kotak VC, Takesian AE, Sanes DH (2008) Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb Cortex 18:2098–2108CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kral A, Tillein J, Hubka P et al (2009) Spatiotemporal patterns of cortical activity with bilateral cochlear implants in congenital deafness. J Neurosci 29:811–827CrossRefPubMedGoogle Scholar
  47. Kyweriga M, Stewart W, Cahill C, Wehr M (2014) Synaptic mechanisms underlying interaural level difference selectivity in rat auditory cortex. J Neurophysiol 112:2561–2571CrossRefPubMedPubMedCentralGoogle Scholar
  48. Laback B, Pok S-M, Baumgartner W-D et al (2004) Sensitivity to interaural level and envelope time differences of two bilateral cochlear implant listeners using clinical sound processors. Ear Hear 25:488–500CrossRefPubMedGoogle Scholar
  49. Lee C-C, Middlebrooks JC (2010) Auditory cortex spatial sensitivity sharpens during task performance. Nat Neurosci 14:108–114CrossRefPubMedPubMedCentralGoogle Scholar
  50. Li L, Kelly JB (1992) Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat’s inferior colliculus. J Neurosci 12:4530–4539PubMedGoogle Scholar
  51. Malhotra S, Lomber SG (2007) Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat. J Neurophysiol 97:26–43CrossRefPubMedGoogle Scholar
  52. McLaughlin SA, Higgins NC, Stecker GC (2015) Tuning to binaural cues in human auditory cortex. J Assoc Res Otolaryngol 17:37–53CrossRefPubMedCentralGoogle Scholar
  53. Moore DR, Irvine DR (1981) Development of responses to acoustic interaural intensity differences in the car inferior colliculus. Exp Brain Res 41:301–309PubMedGoogle Scholar
  54. Mrsic-Flogel TD, Schnupp JWH, King AJ (2003) Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex. Nat Neurosci 6:981–988CrossRefPubMedGoogle Scholar
  55. Németh R, Háden GP, Török M, Winkler I (2015) Processing of horizontal sound localization cues in newborn infants. Ear Hear 36:550–556CrossRefPubMedGoogle Scholar
  56. Palomäki KJ, Tiitinen H, Mäkinen V et al (2005) Spatial processing in human auditory cortex: The effects of 3D, ITD, and ILD stimulation techniques. Cognitive Brain Res 24:364–379CrossRefGoogle Scholar
  57. Petacchi A, Laird AR, Fox PT, Bower JM (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Human Brain Mapp 25:118–128CrossRefGoogle Scholar
  58. Petersson KM, Nichols TE, Poline JB, Holmes AP (1999) Statistical limitations in functional neuroimaging II. Signal detection and statistical inference. Philos Trans R Soc B 354:1261–1281CrossRefGoogle Scholar
  59. Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as “asymmetric sampling in time”. Speech Commun 41:245–255CrossRefGoogle Scholar
  60. Poirier P, Lassonde M, Villemure JG et al (1994) Sound localization in hemispherectomized patients. Neuropsychologia 32:541–553CrossRefPubMedGoogle Scholar
  61. Poirier C, Collignon O, DeVolder AG et al (2005) Specific activation of the V5 brain area by auditory motion processing: an fMRI study. Cogn Brain Res 25:650–658CrossRefGoogle Scholar
  62. Ponton CW, Eggermont JJ (2007) Electrophysiological measures of human auditory system maturation. In: Burkard RF, Don M, Eggermont JJ (eds) Relationship with neuroanatomy and behaviour. Lippincott Williams and Wilkins, Philadelphia, pp 385–402Google Scholar
  63. Quittner AL, Barker DH, Snell C et al (2009) Improvements in visual attention in deaf infants and toddlers after cochlear implantation. Audiol Med 5:242–249CrossRefGoogle Scholar
  64. Salloum CAM, Valero J, Wong DE et al (2010) Lateralization of interimplant timing and level differences in children who use bilateral cochlear implants. Ear Hear 31:441–456CrossRefPubMedGoogle Scholar
  65. Sanes DH, Rubel EW (1988) The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8:682–700PubMedGoogle Scholar
  66. Sanes DH, Takács C (1993) Activity-dependent refinement of inhibitory connections. Eur J Neurosci 5:570–574CrossRefPubMedGoogle Scholar
  67. Seeber BU, Fastl H (2008) Localization cues with bilateral cochlear implants. J Acoust Soc Am 123:1030CrossRefPubMedGoogle Scholar
  68. Semple MN, Kitzes LM (1987) Binaural processing of sound pressure level in the inferior colliculus. J Neurophysiol 57:1130–1147CrossRefPubMedGoogle Scholar
  69. Spierer L, Bellmann-Thiran A, Maeder P et al (2009) Hemispheric competence for auditory spatial representation. Brain 132:1953–1966CrossRefPubMedGoogle Scholar
  70. Stecker GC, McLaughlin SA, Higgins NC (2015) Monaural and binaural contributions to interaural-level-difference sensitivity in human auditory cortex. Neuroimage 120:456–466CrossRefPubMedPubMedCentralGoogle Scholar
  71. Steel MM, Papsin BC, Gordon KA (2015) Binaural fusion and listening effort in children who use bilateral cochlear implants: a psychoacoustic and pupillometric study. PLoS ONE 10:e0117611CrossRefPubMedPubMedCentralGoogle Scholar
  72. Takesian AE, Kotak VC, Sanes DH (2009) Developmental hearing loss disrupts synaptic inhibition: implications for auditory processing. Future Neurol 4:331–349CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tillein J, Hubka P, Syed E et al (2010) Cortical representation of interaural time difference in congenital deafness. Cereb Cortex 20:492–506CrossRefPubMedGoogle Scholar
  74. Tillein J, Hubka P, Kral A (2016) Monaural congenital deafness affects aural dominance and degrades binaural processing. Cerebral Cortex 26:1762CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ungan P, Yagcioglu S, Goksoy C (2001) Differences between the N1 waves of the responses to interaural time and intensity disparities: scalp topography and dipole sources. Clin Neurophysiol 112:485–498CrossRefPubMedGoogle Scholar
  76. Utevsky AV, Smith DV, Huettel SA (2014) Precuneus is a functional core of the default-mode network. J Neurosci 34:932–940CrossRefPubMedPubMedCentralGoogle Scholar
  77. Vale C, Sanes DH (2000) Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J Neurosci Methods 20:1912–1921Google Scholar
  78. van Hoesel R, Ramsden R, Odriscoll M (2002) Sound-direction identification, interaural time delay discrimination, and speech intelligibility advantages in noise for a bilateral cochlear implant user. Ear Hear 23:137–149CrossRefPubMedGoogle Scholar
  79. Van Deun L, van Wieringen A, Van den Bogaert T et al (2009) Sound localization, sound lateralization, and binaural masking level differences in young children with normal hearing. Ear Hear 30:178–190CrossRefPubMedGoogle Scholar
  80. Weeks RA, Aziz-Sultan A, Bushara KO et al (1999) A PET study of human auditory spatial processing. Neurosci Lett 262:155–158CrossRefPubMedGoogle Scholar
  81. Wiggins IM, Seeber BU (2011) Dynamic-range compression affects the lateral position of sounds. J Acoust Soc Am 130:3939–3953CrossRefPubMedGoogle Scholar
  82. Wilke M, Holland SK, Altaye M, Gaser C (2008) Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 41:903–913CrossRefPubMedGoogle Scholar
  83. Wong DE, Gordon KA (2009) Beamformer suppression of cochlear implant artifacts in an electroencephalography dataset. IEEE Trans Biomed Eng 56:2851–2857CrossRefPubMedGoogle Scholar
  84. Yamazaki H, Easwar V, Polonenko M, Jiwani S, Wong DE, Papsin B, Gordon K (Unpublished observation) Development of right hemispheric specialization to monaural tone-bursts from early childhood. Revised manuscript submittedGoogle Scholar
  85. Yucel E, Derim D (2008) The effect of implantation age on visual attention skills. Int J Pediatr Otorhinolaryngol 72:869–877CrossRefPubMedGoogle Scholar
  86. Zatorre RJ, Ptito A, Villemure JG (1995) Preserved auditory spatial localization following cerebral hemispherectomy. Brain 118(Pt 4):879–889CrossRefPubMedGoogle Scholar
  87. Zhang J, Nakamoto KT, Kitzes LM (2004) Binaural interaction revisited in the cat primary auditory cortex. J Neurophysiol 91:101–117CrossRefPubMedGoogle Scholar
  88. Zimmer U, Lewald J, Erb M et al (2004) Is there a role of visual cortex in spatial hearing? Eur J Neurosci 20:3148–3156CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Archie’s Cochlear Implant LaboratoryThe Hospital for Sick ChildrenTorontoCanada
  2. 2.Collaborative Program in NeuroscienceUniversity of TorontoTorontoCanada
  3. 3.Department of OtolaryngologyUniversity of TorontoTorontoCanada
  4. 4.Department of OtolaryngologyThe Hospital for Sick ChildrenTorontoCanada

Personalised recommendations