Abstract
This study aimed to investigate the alterations of cognition and functional connectivity post noise, and find the progress and neural substrates of noise induced hearing loss (NIHL)-associated cognitive impairment. We exposed rats to 122 dB broad-band noise for 2 h to induce hearing loss and the auditory function was assessed by measuring auditory brainstem response thresholds. Morris water maze test and resting state MRI were computed at 0 day, 1, 3, 6 months post noise to reveal cognitive ability and neural substrate. The interregional connections in the auditory network and default mode network, as well as the connections using the auditory cortex and cingulate cortex as seeds were also examined addtionally. The deficit in spatial learning/memory was only observed at 6 months after noise exposure. The internal connections in the auditory network and default mode network were enhanced at 0 day and decreased at 6 months post noise. The connectivity using the auditory cortex and cingulate cortex as seeds generally followed the rule of “enhancement-normal-decrease-widely decrease”. A new model accounting for arousal, dementia, motor control of NIHL in is proposed. Our study highlights the fundamental flexibility of neural systems, and may also point toward novel therapeutic strategies for treating sensory disorders.
Similar content being viewed by others
Availability of data and materials
Imaging data could be provided upon request.
References
Albers, M. W., Gilmore, G. C., Kaye, J., Murphy, C., Wingfield, A., Bennett, D. A., & Zhang, L. I. (2015). At the interface of sensory and motor dysfunctions and Alzheimer’s disease. Alzheimers & Dementia, 11(1), 70–98. https://doi.org/10.1016/j.jalz.2014.04.514
Ash, J. A., Lu, H., Taxier, L. R., Long, J. M., Yang, Y., Stein, E. A., & Rapp, P. R. (2016). Functional connectivity with the retrosplenial cortex predicts cognitive aging in rats. Proceedings of the National Academy of Sciences of the United States of America, 113(43), 12286–12291. https://doi.org/10.1073/pnas.1525309113
Blazquez Freches, G., Chavarrias, C., & Shemesh, N. (2018). BOLD-fMRI in the mouse auditory pathway. NeuroImage, 165, 265–277. https://doi.org/10.1016/j.neuroimage.2017.10.027
Buzsaki, G., & Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neuroscience, 16(2), 130–138. https://doi.org/10.1038/nn.3304
Chand, G. B., Wu, J., Hajjar, I., & Qiu, D. (2017). Interactions of the Salience Network and Its Subsystems with the Default-Mode and the Central-Executive Networks in Normal Aging and Mild Cognitive Impairment. Brain Connect, 7(7), 401–412. https://doi.org/10.1089/brain.2017.0509
Clemm von Hohenberg, C., Weber-Fahr, W., Lebhardt, P., Ravi, N., Braun, U., Gass, N., & Sartorius, A. (2018). Lateral habenula perturbation reduces default-mode network connectivity in a rat model of depression. Translational Psychiatry, 8(1), 68. https://doi.org/10.1038/s41398-018-0121-y
Dewey, R. S., & Hartley, D. E. H. (2015). Cortical cross-modal plasticity following deafness measured using functional near-infrared spectroscopy. Hearing Research, 325, 55–63. https://doi.org/10.1016/j.heares.2015.03.007
Gallagher, M., Burwell, R., & Burchinal, M. (1993). Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behavioral Neuroscience, 107(4), 618–626.
Hsu, L. M., Liang, X., Gu, H., Brynildsen, J. K., Stark, J. A., Ash, J. A., & Yang, Y. (2016). Constituents and functional implications of the rat default mode network. Proceedings of the National Academy of Sciences of the United States of America, 113(31), E4541-4547. https://doi.org/10.1073/pnas.1601485113
Huang, C., & Liu, G. (1990). Organization of the auditory area in the posterior cerebellar vermis of the cat. Experimental Brain Research, 81(2), 377–383.
Hunter, R. G., Gagnidze, K., McEwen, B. S., & Pfaff, D. W. (2015). Stress and the dynamic genome: Steroids, epigenetics, and the transposome. Proceedings of the National Academy of Sciences of the United States of America, 112(22), 6828–6833. https://doi.org/10.1073/pnas.1411260111
Kil, J., Lobarinas, E., Spankovich, C., Griffiths, S. K., Antonelli, P. J., Lynch, E. D., & Le Prell, C. G. (2017). Safety and efficacy of ebselen for the prevention of noise-induced hearing loss: A randomised, double-blind, placebo-controlled, phase 2 trial. Lancet, 390(10098), 969–979. https://doi.org/10.1016/S0140-6736(17)31791-9
Li, P., Shan, H., Liang, S., Nie, B., Duan, S., Huang, Q., & Liu, H. (2018). Structural and functional brain network of human retrosplenial cortex. Neuroscience Letters, 674, 24–29. https://doi.org/10.1016/j.neulet.2018.03.016
Lin, F. R. (2011). Hearing Loss and Cognition Among Older Adults in the United States. Journals of Gerontology Series a-Biological Sciences and Medical Sciences, 66(10), 1131–1136. https://doi.org/10.1093/gerona/glr115
Lin, F. R., Ferrucci, L., An, Y., Goh, J. O., Doshi, J., Metter, E. J., & Resnick, S. M. (2014). Association of hearing impairment with brain volume changes in older adults. NeuroImage, 90, 84–92. https://doi.org/10.1016/j.neuroimage.2013.12.059
Lin, F. R., Metter, E. J., O’Brien, R. J., Resnick, S. M., Zonderman, A. B., & Ferrucci, L. (2011). Hearing loss and incident dementia. Archives of Neurology, 68(2), 214–220. https://doi.org/10.1001/archneurol.2010.362
Lin, F. R., Yaffe, K., Xia, J., Xue, Q., Harris, T. B., Purchase-Helzner, E., & Simonsick, E. M. (2012). Hearing Loss and Cognitive Decline among Older Adults. The Gerontologist, 52, 508–508.
Liu, L., Shen, P., He, T., Chang, Y., Shi, L., Tao, S., & Wang, J. (2016). Noise induced hearing loss impairs spatial learning/memory and hippocampal neurogenesis in mice. Science and Reports, 6, 20374. https://doi.org/10.1038/srep20374
Lu, C. Q., Zeng, C. H., Cui, Y., Meng, X. P., Luan, Y., Xu, X. M., & Ju, S. (2021). An Investigation of the Impacts of Three Anesthetic Regimens on Task-Functional Magnetic Resonance Imaging and Functional Connectivity Resting-State Functional Magnetic Resonance Imaging in Sprague Dawley and Wistar Rats. Brain Connect. https://doi.org/10.1089/brain.2020.0875
Lu, H., Zou, Q., Gu, H., Raichle, M. E., Stein, E. A., & Yang, Y. (2012). Rat brains also have a default mode network. Proceedings of the National Academy of Sciences of the United States of America, 109(10), 3979–3984.
Morris, R. G., Garrud, P., Rawlins, J. N., & O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681–683.
Nasrallah, F. A., To, X. V., Chen, D. Y., Routtenberg, A., & Chuang, K. H. (2016). Functional connectivity MRI tracks memory networks after maze learning in rodents. NeuroImage, 127, 196–202. https://doi.org/10.1016/j.neuroimage.2015.08.013
Nelson, D. I., Nelson, R. Y., Concha-Barrientos, M., & Fingerhut, M. (2005). The global burden of occupational noise-induced hearing loss. American Journal of Industrial Medicine, 48(6), 446–458. https://doi.org/10.1002/ajim.20223
Ortiz-Rios, M., Azevedo, F. A., Kuśmierek, P., Balla, D. Z., Munk, M. H., Keliris, G. A., & Rauschecker, J. P. (2017). Widespread and Opponent fMRI Signals Represent Sound Location in Macaque Auditory Cortex. Neuron, 93(4), 971–983 e974. https://doi.org/10.1016/j.neuron.2017.01.013
Petacchi, A., Laird, A. R., Fox, P. T., & Bower, J. M. (2005). Cerebellum and auditory function: An ALE meta-analysis of functional neuroimaging studies. Human Brain Mapping, 25(1), 118–128. https://doi.org/10.1002/hbm.20137
Porter, B. A., Khodaparast, N., Fayyaz, T., Cheung, R. J., Ahmed, S. S., Vrana, W. A., & Kilgard, M. P. (2012). Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex. Cerebral Cortex, 22(10), 2365–2374. https://doi.org/10.1093/cercor/bhr316
Rambold, H., Churchland, A., Selig, Y., Jasmin, L., & Lisberger, S. G. (2002). Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. Journal of Neurophysiology, 87(2), 912–924.
Rauschecker, J. P., Leaver, A. M., & Muhlau, M. (2010). Tuning out the noise: Limbic-auditory interactions in tinnitus. Neuron, 66(6), 819–826. https://doi.org/10.1016/j.neuron.2010.04.032
Saunders, J. C., Dear, S. P., & Schneider, M. E. (1985). The anatomical consequences of acoustic injury: A review and tutorial. Journal of the Acoustical Society of America, 78(3), 833–860.
Stahl, S. M. (2017). Does treating hearing loss prevent or slow the progress of dementia? Hearing is not all in the ears, but who’s listening? Cns Spectrums, 22(3), 247–250. https://doi.org/10.1017/S1092852917000268
Todd, T. P., Mehlman, M. L., Keene, C. S., DeAngeli, N. E., & Bucci, D. J. (2016). Retrosplenial cortex is required for the retrieval of remote memory for auditory cues. Learning & Memory, 23(6), 278–288. https://doi.org/10.1101/lm.041822
Tsurugizawa, T., & Yoshimaru, D. (2021). Impact of anesthesia on static and dynamic functional connectivity in mice. NeuroImage, 241, 118413. https://doi.org/10.1016/j.neuroimage.2021.118413
van Groen, T., & Wyss, J. M. (1992). Connections of the retrosplenial dysgranular cortex in the rat. The Journal of Comparative Neurology, 315(2), 200–216. https://doi.org/10.1002/cne.903150207
Vann, S. D., Aggleton, J. P., & Maguire, E. A. (2009). What does the retrosplenial cortex do? Nature Reviews Neuroscience, 10(11), 792-U750. https://doi.org/10.1038/nrn2733
Xu, X. M., Jiao, Y., Tang, T. Y., Zhang, J., Lu, C. Q., Salvi, R., & Teng, G. J. (2019a). Sensorineural hearing loss and cognitive impairments: Contributions of thalamus using multiparametric MRI. Journal of Magnetic Resonance Imaging. https://doi.org/10.1002/jmri.26665
Xu, X. M., Jiao, Y., Tang, T. Y., Zhang, J., Salvi, R., & Teng, G. J. (2019b). Inefficient Involvement of Insula in Sensorineural Hearing Loss. Frontiers in Neuroscience, 13, 133. https://doi.org/10.3389/fnins.2019.00133
Yamada, Y., Denkinger, M. D., Onder, G., Henrard, J. C., van der Roest, H. G., Finne-Soveri, H., & Topinkova, E. (2016). Dual Sensory Impairment and Cognitive Decline: The Results From the Shelter Study. Journals of Gerontology. Series a, Biological Sciences and Medical Sciences, 71(1), 117–123. https://doi.org/10.1093/gerona/glv036
Yang, M., Chen, H. J., Liu, B., Huang, Z. C., Feng, Y., Li, J., & Teng, G. J. (2014). Brain structural and functional alterations in patients with unilateral hearing loss. Hearing Research, 316, 37–43. https://doi.org/10.1016/j.heares.2014.07.006
Zhao, S., Shetty, J., Hou, L., Delcher, A., Zhu, B., Osoegawa, K., & Fraser, C. M. (2004). Human, mouse, and rat genome large-scale rearrangements: Stability versus speciation. Genome Research, 14(10A), 1851–1860. https://doi.org/10.1101/gr.2663304
Funding
This work was supported by the National Natural Science Foundation of China (81520108015), Doctoral Program of Entrepreneurship and Innovation in Jiangsu Province (JSSCBS20211544) and Xinghuo Talent Program of Nanjing First Hospital.
Author information
Authors and Affiliations
Contributions
XMX, conducted the noise exposure and hearing ability tests, collected the fMRI data, performed the analysis, and wrote the manuscript; YQZ helped with the MRI scanning and conclusion; FCZ and CQL contributed to fMRI data analysis; LJL contributed the analysis of the behavioral test and discussion; JW and RS helped with revision; GJT and YCC helped design the MRI experiment and manuscript revision. GJT and YCC are co- corresponding authors of this paper.
Corresponding authors
Ethics declarations
Ethics approval
All animal procedures were conducted in accordance with the Institutional Animal Care and Use Committee (IACUC), as well as the National Institutes of Health Guide for the Care and Use of Laboratory Animals and approved by the Animal Care Committee of our University.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, XM., Zhang, YQ., Zang, FC. et al. Alterations to cognitive abilities and functional networks in rats post broad-band intense noise exposure. Brain Imaging and Behavior 16, 1884–1892 (2022). https://doi.org/10.1007/s11682-022-00643-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-022-00643-8