Developmental Exposure to Polychlorinated Biphenyls Prevents Recovery from Noise-Induced Hearing Loss and Disrupts the Functional Organization of the Inferior Colliculus.

Autor:	Ibrahim BA; Department of Molecular and Integrative Physiology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Louie JJ; Department of Molecular and Integrative Physiology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Shinagawa Y; Department of Molecular and Integrative Physiology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Xiao G; Department of Molecular and Integrative Physiology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Asilador AR; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Sable HJK; The Department of Psychology, The University of Memphis, Memphis, Tennessee 38152., Schantz SL; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Department of Comparative Biosciences, University of Illinois Urbana-Champaign, Urbana, Illinois 61801., Llano DA; Department of Molecular and Integrative Physiology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801 d-llano@illinois.edu.; Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.; Carle Illinois College of Medicine, University of Illinois Urbana-Champaign, Urbana, Illinois 61801.
Jazyk:	angličtina
Zdroj:	The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2023 Jun 21; Vol. 43 (25), pp. 4580-4597. Date of Electronic Publication: 2023 May 05.
DOI:	10.1523/JNEUROSCI.0030-23.2023
Abstrakt:	Exposure to combinations of environmental toxins is growing in prevalence; and therefore, understanding their interactions is of increasing societal importance. Here, we examined the mechanisms by which two environmental toxins, polychlorinated biphenyls (PCBs) and high-amplitude acoustic noise, interact to produce dysfunction in central auditory processing. PCBs are well established to impose negative developmental impacts on hearing. However, it is not known whether developmental exposure to this ototoxin alters the sensitivity to other ototoxic exposures later in life. Here, male mice were exposed to PCBs in utero, and later as adults were exposed to 45 min of high-intensity noise. We then examined the impacts of the two exposures on hearing and the organization of the auditory midbrain using two-photon imaging and analysis of the expression of mediators of oxidative stress. We observed that developmental exposure to PCBs blocked hearing recovery from acoustic trauma. In vivo two-photon imaging of the inferior colliculus (IC) revealed that this lack of recovery was associated with disruption of the tonotopic organization and reduction of inhibition in the auditory midbrain. In addition, expression analysis in the inferior colliculus revealed that reduced GABAergic inhibition was more prominent in animals with a lower capacity to mitigate oxidative stress. These data suggest that combined PCBs and noise exposure act nonlinearly to damage hearing and that this damage is associated with synaptic reorganization, and reduced capacity to limit oxidative stress. In addition, this work provides a new paradigm by which to understand nonlinear interactions between combinations of environmental toxins. SIGNIFICANCE STATEMENT Exposure to common environmental toxins is a large and growing problem in the population. This work provides a new mechanistic understanding of how the prenatal and postnatal developmental changes induced by polychlorinated biphenyls (PCBs) could negatively impact the resilience of the brain to noise-induced hearing loss (NIHL) later in adulthood. The use of state-of-the-art tools, including in vivo multiphoton microscopy of the midbrain helped in identifying the long-term central changes in the auditory system after the peripheral hearing damage induced by such environmental toxins. In addition, the novel combination of methods employed in this study will lead to additional advances in our understanding of mechanisms of central hearing loss in other contexts. (Copyright © 2023 the authors.)
Databáze:	MEDLINE
Externí odkaz:	Zobrazit plný text záznamu