Skip to main content
Log in

Decoding auditory deprivation: resting-state fMRI insights into deafness and brain plasticity

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Deafness, as a profound manifestation of sensory deprivation, prompts a cascade of intricate cerebral adaptations. In this study, involving 35 deaf individuals and 35 hearing controls, we utilized resting-state functional magnetic resonance imaging (rs-fMRI) to delve into the depths of functional connectivity nuances distinguishing deaf individuals from their hearing counterparts. Leading our analytical approach was the application of multi-voxel pattern analysis (fc-MVPA). This advanced method provided a refined perspective, revealing amplified neural connectivity within the deaf population. Notably, regions such as the left postcentral somatosensory association cortex, the anterior and posterior corridors of the left superior temporal gyrus (STG), and the left mid-temporal lobe were identified as hotspots of heightened connectivity. Further, fc-MVPA shed light on intricate interaction effects, which became more pronounced when examining variables such as the duration of auditory deprivation and the extent of sign language exposure. These interactions were particularly evident in the premotor and left frontal mid-orbital regions. Complementing this, seed-based connectivity assessments illuminated pronounced coupling dynamics within the left STG spectrum. Concurrently, local correlation (LCOR) value analysis in the deaf group revealed significant shifts in the right superior STG and bilateral precuneus. In addition, amplitude of low-frequency fluctuation (ALFF) evaluations indicated modulations in the bilateral mid cingulum and left superior mid frontal gyrus. This comprehensive, fc-MVPA-driven exploration uncovers the multifaceted functional adaptations resulting from deafness, highlighting the profound plasticity of the human brain and its potential implications for targeted rehabilitative strategies.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Inquiries about data availability should be directed to the authors.

References

  • Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3(6):443–452

    Article  CAS  PubMed  Google Scholar 

  • Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19(12):2767–2796

    Article  PubMed  PubMed Central  Google Scholar 

  • Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541

    Article  CAS  PubMed  Google Scholar 

  • Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(3):564–583

    Article  PubMed  Google Scholar 

  • Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3(3):292–297

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70

    Article  CAS  PubMed  Google Scholar 

  • Deshpande G, LaConte S, Peltier S, Hu X (2009) Integrated local correlation: a new measure of local coherence in fMRI data. Hum Brain Mapp 30(1):13–23

    Article  PubMed  Google Scholar 

  • Desimone R, Ungerleider LG (1989) Neural mechanisms of visual processing in monkeys. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 2. Elsevier, Amsterdam, pp 267–299

    Google Scholar 

  • Emmorey K, Allen JS, Bruss J, Schenker N, Damasio H (2007a) A morphometric analysis of auditory brain regions in congenitally deaf adults. Proc Natl Acad Sci 104(17):12193–12198

    Google Scholar 

  • Emmorey K, Mehta S, Grabowski TJ (2007b) The neural correlates of sign versus word production. Neuroimage 36(1):202–208

    Article  PubMed  Google Scholar 

  • Emmorey K, McCullough S, Weisberg J (2014) Neural correlates of fingerspelling, text, and sign processing in deaf American Sign Language-English bilinguals. Linguist Var 14(2):237–253

    Google Scholar 

  • Fine I, Finney EM, Boynton GM, Dobkins KR (2005) Comparing the effects of auditory deprivation and sign language within the auditory and visual cortex. J Cognit Neurosci 17(10):1621–1637

    Article  Google Scholar 

  • Finney EM, Fine I, Dobkins KR (2001) Visual stimuli activate auditory cortex in the deaf. Nat Neurosci 4(12):1171–1173

    Article  CAS  PubMed  Google Scholar 

  • Gong W, Cheng F, Rolls ET, Lo CYZ, Huang CC, Tsai SJ, Yang AC, Lin C-P, Feng J (2019) A powerful and efficient multivariate approach for voxel-level connectome-wide association studies. NeuroImage 188:628–641

    Article  PubMed  Google Scholar 

  • Grill-Spector K, Malach R (2004) The human visual cortex. Annu Rev Neurosci 27:649–677

    Article  CAS  PubMed  Google Scholar 

  • Haynes JD, Rees G (2006) Decoding mental states from brain activity in humans. Nat Rev Neurosci 7(7):523–534

    Article  CAS  PubMed  Google Scholar 

  • Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402

    Article  CAS  PubMed  Google Scholar 

  • Kral A, Sharma A (2012) Developmental neuroplasticity after cochlear implantation. Trends Neurosci 35(2):111–122

    Article  CAS  PubMed  Google Scholar 

  • Kumar U, Keshri A, Mishra M (2021) Alteration of brain resting-state networks and functional connectivity in prelingual deafness. J Neuroimaging 31(6):1135–1145

    Article  PubMed  Google Scholar 

  • Kumar U, Arya A, Agarwal V (2022) Altered functional connectivity in children with ADHD while performing cognitive control task. Psychiatry Res Neuroimaging 326:111531

    Article  PubMed  Google Scholar 

  • Lee DS, Lee JS, Oh SH, Kim SK, Kim JW, Chung JK, Lee MC, Kim CS (2001) Cross-modal plasticity and cochlear implants. Nature 409(6817):149–150

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Ding G, Booth JR, Huang R, Lv Y, Zang Y, He Y, Peng D (2012) Sensitive period for white-matter connectivity of superior temporal cortex in deaf people. Hum Brain Mapp 33(2):349–359

    Article  PubMed  Google Scholar 

  • Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13(11):1421–1427

    Article  CAS  PubMed  Google Scholar 

  • Lyness CR, Woll B, Campbell R, Cardin V (2013) How does visual language affect crossmodal plasticity and cochlear implant success? Neurosci Biobehav Rev 37(10):2621–2630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239

    Article  PubMed  Google Scholar 

  • McCullough S, Emmorey K (2021) Effects of deafness and sign language experience on the human brain: voxel-based and surface-based morphometry. Lang Cognit Neurosci 36(4):422–439

    Article  Google Scholar 

  • Merabet LB, Pascual-Leone A (2010) Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 11(1):44–52

    Article  CAS  PubMed  Google Scholar 

  • Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1996) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224(4):591–605

    Article  Google Scholar 

  • Neubauer AC, Fink A (2009) Intelligence and neural efficiency. Neurosci Biobehav Rev 33(7):1004–1023

    Article  PubMed  Google Scholar 

  • Nieto-Castanon A (2022) Brain-wide connectome inferences using functional connectivity MultiVariate pattern analyses (fc-MVPA). PLoS Comput Biol 18(11):e1010634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura H, Hashikawa K, Doi K, Iwaki T, Watanabe Y, Kusuoka H, Nishimura T, Kubo T (1999) Sign language ‘heard’ in the auditory cortex. Nature 397(6715):116

    Article  CAS  PubMed  Google Scholar 

  • Novick JM, Trueswell JC, Thompson-Schill SL (2005) Cognitive control and parsing: reexamining the role of Broca’s area in sentence comprehension. Cogn Affect Behav Neurosci 5(3):263–281

    Article  PubMed  Google Scholar 

  • Paulesu E, Frith CD, Frackowiak RS (1993) The neural correlates of the verbal component of working memory. Nature 362(6418):342–345

    Article  CAS  PubMed  Google Scholar 

  • Philip R et al (2018) Cross-validation strategies in neuroimaging: benefits and implications for interpretability. Neuroimage 173:15–21

    Google Scholar 

  • Ridderinkhof KR, Van Den Wildenberg WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cognit 56(2):129–140

    Article  Google Scholar 

  • Rosazza C, Aquino D, D’Incerti L, Cordella R, Andronache A, Zacà D, Bruzzone MG, Tringali G, Minati L (2014) Preoperative mapping of the sensorimotor cortex: comparative assessment of task-based and resting-state FMRI. PLoS One 9(6):e98860

    Article  PubMed  PubMed Central  Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069

    Article  PubMed  Google Scholar 

  • Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Nat Acad Sci 106(31):13040–13045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15(4):3215–3230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzourio-Mazoyer N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289

    Article  CAS  PubMed  Google Scholar 

  • Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6(7):533–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56(2):366–383

    Article  CAS  PubMed  Google Scholar 

  • Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2(3):125–141

    Article  PubMed  Google Scholar 

  • Ying J, Li C, Yuan T, Jin L, Wang R, Zuo Z, Zhang Y (2019) Increased resting-state functional connectivity in suprasellar tumor patients with postoperative visual improvement. Int J Med Sci 16(9):1245

    Article  PubMed  PubMed Central  Google Scholar 

  • Zang Y, Jiang T, Lu Y, He Y, Tian L (2007) Regional homogeneity approach to fMRI data analysis. Neuroimage 22(1):394–400

    Article  Google Scholar 

  • Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, Wang YF, Zang YF (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172(1):137–141

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We express our gratitude to the Department of Science and Technology for their generous funding (grant no. DST/CSRI/2018/114).

Funding

This study was supported by the Department of Science and Technology, Ministry of Science and Technology, India (grant no. DST/CSRI/2018/114).

Author information

Authors and Affiliations

Authors

Contributions

UK contributed to the conceptualization of the study, data acquisition, analysis of fMRI data, and drafting of the manuscript. KD played a significant role in the design of the study, data acquisition, and interpretation of the results. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Uttam Kumar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, U., Dhanik, K. Decoding auditory deprivation: resting-state fMRI insights into deafness and brain plasticity. Brain Struct Funct 229, 729–740 (2024). https://doi.org/10.1007/s00429-023-02757-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-023-02757-1

Keywords

Navigation