Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • 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–EL92

    Article  PubMed  PubMed Central  Google Scholar 

  • 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–EL387

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashmead DH, Davis DL, Whalen T, Odom RD (1991) Sound localization and sensitivity to interaural time differences in human infants. Child Dev 62:1211–1226

    Article  CAS  PubMed  Google Scholar 

  • Baumann O, Mattingley JB (2010) Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci Methods 30:4489–4495

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Blair RC, Karniski W (1993) An alternative method for significance testing of waveform difference potentials. Psychophysiology 30:518–524

    Article  CAS  PubMed  Google Scholar 

  • Blatchley BJ, Brugge JF (1990) Sensitivity to binaural intensity and phase difference cues in kitten inferior colliculus. J Neurophysiol 64:582–597

    Article  CAS  PubMed  Google Scholar 

  • Brugge JF, Reale RA, Wilson GF (1988) Sensitivity of auditory cortical neurons of kittens to monaural and binaural high frequency sound. Hear Res 34:127–140

    Article  CAS  PubMed  Google Scholar 

  • 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 26:251–261

    Article  CAS  Google Scholar 

  • Bundy RS (1980) Discrimination of sound localization cues in young infants. Child Dev 51:292–294

    Article  CAS  PubMed  Google Scholar 

  • 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 2:759–766

    Article  CAS  PubMed  Google Scholar 

  • 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 95:3742–3755

    Article  PubMed  Google Scholar 

  • Cavanna AE, Trimble M (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583

    Article  PubMed  Google Scholar 

  • Chau W, McIntosh AR, Robinson SE et al (2004) Improving permutation test power for group analysis of spatially filtered MEG data. Neuroimage 23:983–996

    Article  PubMed  Google Scholar 

  • 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 20:1454–1463

    Article  PubMed  Google Scholar 

  • 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 106:163–178

    Article  CAS  PubMed  Google Scholar 

  • Dalal SS, Sekihara K, Nagarajan SS (2006) Modified beamformers for coherent source region suppression. IEEE Trans Biomed Eng 53:1357–1363

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 23:352–355

    PubMed  Google Scholar 

  • Ducommun CY, Murray MM, Thut G et al (2002) Segregated processing of auditory motion and auditory location: an ERP mapping study. Neuroimage 16:76–88

    Article  PubMed  Google Scholar 

  • Easwar V, Sanfilippo J, Papsin BC, Gordon KA (2016) Factors affecting daily cochlear implant use inchildren: datalogging evidence. J Am Acad Audiol 27:824–838

    Article  PubMed  Google Scholar 

  • 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 37:2349–2361

    Article  CAS  PubMed  Google Scholar 

  • 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–e00615

    Article  Google Scholar 

  • 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 154:346–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon KA, Papsin BC (2013) From nucleus 24 to 513: changing cochlear implant design affects auditory response thresholds. Otol Neurotol 34:436–442

    Article  PubMed  Google Scholar 

  • 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 118:1671–1684

    Article  CAS  PubMed  Google Scholar 

  • 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 122:823–833

    Article  CAS  PubMed  Google Scholar 

  • 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 32:4212–4223

    Article  CAS  PubMed  Google Scholar 

  • Gordon KA, Wong DE, Papsin BC (2013) Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf. Brain 136:1609–1625

    Article  PubMed  Google Scholar 

  • 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:e114841

    Article  PubMed  PubMed Central  Google Scholar 

  • Gordon KA, Henkin Y, Kral A (2015) Asymmetric hearing during development: the aural preference syndrome and treatment options. Pediatrics 136:141–153

    Article  PubMed  Google Scholar 

  • Gordon KA, Abbasalipour P, Papsin BC (2016) Balancing current levels in children with bilateral cochlear implants using electrophysiological and behavioural measures. Hear Res 335:193–206

    Article  PubMed  Google Scholar 

  • 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 28:524–541

    Article  PubMed  Google Scholar 

  • 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 29:33–44

    PubMed  Google Scholar 

  • Griffiths TD, Rees G, Rees A et al (1998) Right parietal cortex is involved in the perception of sound movement in humans. Nat Neurosci 1:74–79

    Article  CAS  PubMed  Google Scholar 

  • Grothe B, Pecka M (2014) The natural history of sound localization in mammals: a story of neuronal inhibition. Front Neural Circuits 8:1–19

    Article  Google Scholar 

  • 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 30:14068–14079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann R, Topp G, Klinke R (1984) Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea. Hear Res 13:47–62

    Article  CAS  PubMed  Google Scholar 

  • Jiwani S, Papsin BC, Gordon KA (2016) Early unilateral cochlear implantation promotes mature cortical asymmetries in adoloscents who are deaf. Human Brain Mapp 37:135–152

    Article  Google Scholar 

  • Johnson BW, Hautus MJ (2010) Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 48:2610–2619

    Article  PubMed  Google Scholar 

  • 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 44:541–551

    Article  PubMed  Google Scholar 

  • Kaga M (1992) Development of sound localization. Acta Paediatr Jpn 34:134–138

    Article  CAS  PubMed  Google Scholar 

  • Kan A, Litovsky RY (2015) Binaural hearing with electrical stimulation. Hear Res 322:127–137

    Article  PubMed  Google Scholar 

  • Koch U, Sanes DH (1998) Afferent regulation of glycine receptor distribution in the gerbil LSO. Microsc Res Tech 41:263–269

    Article  CAS  PubMed  Google Scholar 

  • Kotak VC, Sanes DH (1996) Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J Neurosci 16:1836–1843

    CAS  PubMed  Google Scholar 

  • Kotak VC, Takesian AE, Sanes DH (2008) Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb Cortex 18:2098–2108

    Article  PubMed  PubMed Central  Google Scholar 

  • Kral A, Tillein J, Hubka P et al (2009) Spatiotemporal patterns of cortical activity with bilateral cochlear implants in congenital deafness. J Neurosci 29:811–827

    Article  CAS  PubMed  Google Scholar 

  • Kyweriga M, Stewart W, Cahill C, Wehr M (2014) Synaptic mechanisms underlying interaural level difference selectivity in rat auditory cortex. J Neurophysiol 112:2561–2571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:488–500

    Article  PubMed  Google Scholar 

  • Lee C-C, Middlebrooks JC (2010) Auditory cortex spatial sensitivity sharpens during task performance. Nat Neurosci 14:108–114

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 12:4530–4539

    CAS  PubMed  Google Scholar 

  • 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 97:26–43

    Article  PubMed  Google Scholar 

  • McLaughlin SA, Higgins NC, Stecker GC (2015) Tuning to binaural cues in human auditory cortex. J Assoc Res Otolaryngol 17:37–53

    Article  PubMed Central  Google Scholar 

  • Moore DR, Irvine DR (1981) Development of responses to acoustic interaural intensity differences in the car inferior colliculus. Exp Brain Res 41:301–309

    CAS  PubMed  Google Scholar 

  • Mrsic-Flogel TD, Schnupp JWH, King AJ (2003) Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex. Nat Neurosci 6:981–988

    Article  CAS  PubMed  Google Scholar 

  • Németh R, Háden GP, Török M, Winkler I (2015) Processing of horizontal sound localization cues in newborn infants. Ear Hear 36:550–556

    Article  PubMed  Google Scholar 

  • 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 24:364–379

    Article  Google Scholar 

  • Petacchi A, Laird AR, Fox PT, Bower JM (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Human Brain Mapp 25:118–128

    Article  Google Scholar 

  • 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 354:1261–1281

    Article  CAS  Google Scholar 

  • Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as “asymmetric sampling in time”. Speech Commun 41:245–255

    Article  Google Scholar 

  • Poirier P, Lassonde M, Villemure JG et al (1994) Sound localization in hemispherectomized patients. Neuropsychologia 32:541–553

    Article  CAS  PubMed  Google Scholar 

  • 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 25:650–658

    Article  Google Scholar 

  • 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 385–402

    Google Scholar 

  • Quittner AL, Barker DH, Snell C et al (2009) Improvements in visual attention in deaf infants and toddlers after cochlear implantation. Audiol Med 5:242–249

    Article  Google Scholar 

  • 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 31:441–456

    Article  PubMed  Google Scholar 

  • Sanes DH, Rubel EW (1988) The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8:682–700

    CAS  PubMed  Google Scholar 

  • Sanes DH, Takács C (1993) Activity-dependent refinement of inhibitory connections. Eur J Neurosci 5:570–574

    Article  CAS  PubMed  Google Scholar 

  • Seeber BU, Fastl H (2008) Localization cues with bilateral cochlear implants. J Acoust Soc Am 123:1030

    Article  PubMed  Google Scholar 

  • Semple MN, Kitzes LM (1987) Binaural processing of sound pressure level in the inferior colliculus. J Neurophysiol 57:1130–1147

    Article  CAS  PubMed  Google Scholar 

  • Spierer L, Bellmann-Thiran A, Maeder P et al (2009) Hemispheric competence for auditory spatial representation. Brain 132:1953–1966

    Article  PubMed  Google Scholar 

  • Stecker GC, McLaughlin SA, Higgins NC (2015) Monaural and binaural contributions to interaural-level-difference sensitivity in human auditory cortex. Neuroimage 120:456–466

    Article  PubMed  PubMed Central  Google Scholar 

  • 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:e0117611

    Article  PubMed  PubMed Central  Google Scholar 

  • Takesian AE, Kotak VC, Sanes DH (2009) Developmental hearing loss disrupts synaptic inhibition: implications for auditory processing. Future Neurol 4:331–349

    Article  PubMed  PubMed Central  Google Scholar 

  • Tillein J, Hubka P, Syed E et al (2010) Cortical representation of interaural time difference in congenital deafness. Cereb Cortex 20:492–506

    Article  CAS  PubMed  Google Scholar 

  • Tillein J, Hubka P, Kral A (2016) Monaural congenital deafness affects aural dominance and degrades binaural processing. Cerebral Cortex 26:1762

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 112:485–498

    Article  CAS  PubMed  Google Scholar 

  • Utevsky AV, Smith DV, Huettel SA (2014) Precuneus is a functional core of the default-mode network. J Neurosci 34:932–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vale C, Sanes DH (2000) Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J Neurosci Methods 20:1912–1921

    CAS  Google Scholar 

  • 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 23:137–149

    Article  PubMed  Google Scholar 

  • 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 30:178–190

    Article  PubMed  Google Scholar 

  • Weeks RA, Aziz-Sultan A, Bushara KO et al (1999) A PET study of human auditory spatial processing. Neurosci Lett 262:155–158

    Article  CAS  PubMed  Google Scholar 

  • Wiggins IM, Seeber BU (2011) Dynamic-range compression affects the lateral position of sounds. J Acoust Soc Am 130:3939–3953

    Article  PubMed  Google Scholar 

  • Wilke M, Holland SK, Altaye M, Gaser C (2008) Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 41:903–913

    Article  PubMed  Google Scholar 

  • Wong DE, Gordon KA (2009) Beamformer suppression of cochlear implant artifacts in an electroencephalography dataset. IEEE Trans Biomed Eng 56:2851–2857

    Article  PubMed  Google Scholar 

  • 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 submitted

  • Yucel E, Derim D (2008) The effect of implantation age on visual attention skills. Int J Pediatr Otorhinolaryngol 72:869–877

    Article  PubMed  Google Scholar 

  • Zatorre RJ, Ptito A, Villemure JG (1995) Preserved auditory spatial localization following cerebral hemispherectomy. Brain 118(Pt 4):879–889

    Article  PubMed  Google Scholar 

  • Zhang J, Nakamoto KT, Kitzes LM (2004) Binaural interaction revisited in the cat primary auditory cortex. J Neurophysiol 91:101–117

    Article  PubMed  Google Scholar 

  • Zimmer U, Lewald J, Erb M et al (2004) Is there a role of visual cortex in spatial hearing? Eur J Neurosci 20:3148–3156

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Archie’s Cochlear Implant Laboratory, The Hospital for Sick Children, Room 6D08, 555 University Avenue, Toronto, ON, M5G 1X8, Canada

    Vijayalakshmi Easwar, Hiroshi Yamazaki, Michael Deighton & Karen Gordon

  2. Collaborative Program in Neuroscience, University of Toronto, Toronto, Canada

    Vijayalakshmi Easwar

  3. Department of Otolaryngology, University of Toronto, Toronto, Canada

    Blake Papsin & Karen Gordon

  4. Department of Otolaryngology, The Hospital for Sick Children, Toronto, Canada

    Blake Papsin

Authors
  1. Vijayalakshmi Easwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroshi Yamazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Deighton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Blake Papsin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karen Gordon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vijayalakshmi Easwar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Easwar, V., Yamazaki, H., Deighton, M. et al. Cortical Processing of Level Cues for Spatial Hearing is Impaired in Children with Prelingual Deafness Despite Early Bilateral Access to Sound. Brain Topogr 31, 270–287 (2018). https://doi.org/10.1007/s10548-017-0596-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-017-0596-5

Keywords

Search

Navigation