Dyslexia-Related Hearing Loss Occurs Mainly Through the Abnormal Spontaneous Electrical Activity of Spiral Ganglion Neurons

Overview

Journal Adv Sci (Weinh)

Specialty Biomedical Engineering

Date 2023 Apr 17

PMID 37068190

Authors

Guodong Hong

Xiaolong Fu

Xin Chen

Liyan Zhang

Xuan Han

Shuqin Ding

Ziyi Liu

Xiuli Bi

Wen Li

Miao Chang

Ruifeng Qiao

Siwei Guo

Hailong Tu

Renjie Chai

Affiliations

Soon will be listed here.

Abstract

Dyslexia is a reading and spelling disorder due to neurodevelopmental abnormalities and is occasionally found to be accompanied by hearing loss, but the reason for the associated deafness remains unclear. This study finds that knockout of the dyslexia susceptibility 1 candidate 1 gene (Dyx1c1 ) in mice, the best gene for studying dyslexia, causes severe hearing loss, and thus it is a good model for studying the mechanism of dyslexia-related hearing loss (DRHL). This work finds that the Dyx1c1 gene is highly expressed in the mouse cochlea and that the spontaneous electrical activity of inner hair cells and type I spiral ganglion neurons is altered in the cochleae of Dyx1c1 mice. In addition, primary ciliary dyskinesia-related phenotypes such as situs inversus and disrupted ciliary structure are seen in Dyx1c1 mice. In conclusion, this study gives new insights into the mechanism of DRHL in detail and suggests that Dyx1c1 may serve as a potential target for the clinical diagnosis of DRHL.

Citing Articles

Hong G, Fu X, Chen X, Zhang L, Han X, Ding S Adv Sci (Weinh). 2023; 10(16):e2205754.

PMID: 37068190 PMC: 10238183. DOI: 10.1002/advs.202205754.

References

Kimel E, Weiss A, Jakoby H, Daikhin L, Ahissar M . Short-term memory capacity and sensitivity to language statistics in dyslexia and among musicians. Neuropsychologia. 2020; 149:107624. PMC: 7768182. DOI: 10.1016/j.neuropsychologia.2020.107624. View

Giraud A, Ramus F . Neurogenetics and auditory processing in developmental dyslexia. Curr Opin Neurobiol. 2012; 23(1):37-42. DOI: 10.1016/j.conb.2012.09.003. View

Threlkeld S, Hill C, Cleary C, Truong D, Rosen G, Holly Fitch R . Developmental learning impairments in a rodent model of nodular heterotopia. J Neurodev Disord. 2011; 1(3):237-50. PMC: 3196316. DOI: 10.1007/s11689-009-9026-7. View

Kovelman I, Norton E, Christodoulou J, Gaab N, Lieberman D, Triantafyllou C . Brain basis of phonological awareness for spoken language in children and its disruption in dyslexia. Cereb Cortex. 2011; 22(4):754-64. PMC: 4498147. DOI: 10.1093/cercor/bhr094. View

Rohacek A, Bebee T, Tilton R, Radens C, McDermott-Roe C, Peart N . ESRP1 Mutations Cause Hearing Loss due to Defects in Alternative Splicing that Disrupt Cochlear Development. Dev Cell. 2017; 43(3):318-331.e5. PMC: 5687886. DOI: 10.1016/j.devcel.2017.09.026. View

Rosen G, Bai J, Wang Y, Fiondella C, Threlkeld S, LoTurco J . Disruption of neuronal migration by RNAi of Dyx1c1 results in neocortical and hippocampal malformations. Cereb Cortex. 2007; 17(11):2562-72. PMC: 3742088. DOI: 10.1093/cercor/bhl162. View

Caprara G, Mecca A, Peng A . Decades-old model of slow adaptation in sensory hair cells is not supported in mammals. Sci Adv. 2020; 6(33):eabb4922. PMC: 7428330. DOI: 10.1126/sciadv.abb4922. View

TAIT C, Roush J, Johns J . Normal ABR's in children classified as learning disabled. J Aud Res. 1983; 23(1):56-62. View

Brandt A, Striessnig J, Moser T . CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J Neurosci. 2003; 23(34):10832-40. PMC: 6740966. View

10.

Shaywitz S, Shaywitz B . Dyslexia (specific reading disability). Biol Psychiatry. 2005; 57(11):1301-9. DOI: 10.1016/j.biopsych.2005.01.043. View

11.

Georgiou G, Protopapas A, Papadopoulos T, Skaloumbakas C, Parrila R . Auditory temporal processing and dyslexia in an orthographically consistent language. Cortex. 2010; 46(10):1330-44. DOI: 10.1016/j.cortex.2010.06.006. View

12.

Cowan N, Hogan T, Alt M, Green S, Cabbage K, Brinkley S . Short-term Memory in Childhood Dyslexia: Deficient Serial Order in Multiple Modalities. Dyslexia. 2017; 23(3):209-233. PMC: 5540735. DOI: 10.1002/dys.1557. View

13.

Aprea I, Raidt J, Hoben I, Loges N, Nothe-Menchen T, Pennekamp P . Defects in the cytoplasmic assembly of axonemal dynein arms cause morphological abnormalities and dysmotility in sperm cells leading to male infertility. PLoS Genet. 2021; 17(2):e1009306. PMC: 7909641. DOI: 10.1371/journal.pgen.1009306. View

14.

Grammatikopoulos T, Sambrotta M, Strautnieks S, Foskett P, Knisely A, Wagner B . Mutations in DCDC2 (doublecortin domain containing protein 2) in neonatal sclerosing cholangitis. J Hepatol. 2016; 65(6):1179-1187. PMC: 5116266. DOI: 10.1016/j.jhep.2016.07.017. View

15.

Dixit S, Khanna R . Situs inversus, developmental dyslexia and psychosis. Can J Psychiatry. 1993; 38(4):300-1. DOI: 10.1177/070674379303800421. View

16.

Wang Z, Jung J, Inbar T, Rangoussis K, Faaborg-Andersen C, Coate T . The Purinergic Receptor P2rx3 is Required for Spiral Ganglion Neuron Branch Refinement during Development. eNeuro. 2020; 7(4). PMC: 7418533. DOI: 10.1523/ENEURO.0179-20.2020. View

17.

Diaz R, Kronenberg N, Martinelli A, Liehm P, Riches A, Gather M . KIAA0319 influences cilia length, cell migration and mechanical cell-substrate interaction. Sci Rep. 2022; 12(1):722. PMC: 8760330. DOI: 10.1038/s41598-021-04539-3. View

18.

Wang H, Lin C, Chong R, Zhang-Hooks Y, Agarwal A, Ellis-Davies G . Spontaneous Activity of Cochlear Hair Cells Triggered by Fluid Secretion Mechanism in Adjacent Support Cells. Cell. 2015; 163(6):1348-59. PMC: 4671825. DOI: 10.1016/j.cell.2015.10.070. View

19.

Babola T, Li S, Gribizis A, Lee B, Issa J, Wang H . Homeostatic Control of Spontaneous Activity in the Developing Auditory System. Neuron. 2018; 99(3):511-524.e5. PMC: 6100752. DOI: 10.1016/j.neuron.2018.07.004. View

20.

Cohen-Mimran R, Sapir S . Auditory temporal processing deficits in children with reading disabilities. Dyslexia. 2007; 13(3):175-92. DOI: 10.1002/dys.323. View