Elsevier

Neuroscience

Volume 379, 21 May 2018, Pages 428-434
Neuroscience

Research Article
Blast Exposure Disrupts the Tonotopic Frequency Map in the Primary Auditory Cortex

https://doi.org/10.1016/j.neuroscience.2018.03.041Get rights and content

Highlights

  • Exposure to a 22-psi blast increased response threshold in the auditory cortex.

  • Blast exposure resulted in broadened frequency tuning.

  • Blast exposure resulted in shortened response latency.

  • Blast exposure resulted in distorted cortical frequency map.

Abstract

Blast exposure can cause various auditory disorders including tinnitus, hyperacusis, and other central auditory processing disorders. While this is suggestive of pathologies in the central auditory system, the impact of blast exposure on central auditory processing remains poorly understood. Here we examined the effects of blast shockwaves on acoustic response properties and the tonotopic frequency map in the auditory cortex. We found that multiunits recorded from the auditory cortex exhibited higher acoustic thresholds and broader frequency tuning in blast-exposed animals. Furthermore, the frequency map in the primary auditory cortex was distorted. These changes may contribute to central auditory processing disorders.

Introduction

Exposure to blast shockwaves can cause sensory and neurological disorders in the auditory system, such as hearing loss, tinnitus, hyperacusis and central processing disorder (Jury and Flynn, 2001, Rossiter et al., 2006, Sayer et al., 2008, Belanger et al., 2009, Mao et al., 2012, Remenschneider et al., 2014, Saunders et al., 2015, Bressler et al., 2017, Ouyang et al., 2017). However, the mechanism by which blasts impact the auditory system remains unclear (Rosenfeld and Ford, 2010). Exposure to shockwaves causes damage to the ear, but the impact can be quite different from that of noise exposure (Bauer et al., 2008). Blast shockwaves are brief and often rupture the tympanic membrane, which decouples the inner ear from further mechanical over-stimulation (Xydakis et al., 2007). Consequently, blast exposure often causes severe acute hearing loss, but only mild long-term hearing loss following recovery of the tympanic membrane (Mao et al., 2012, Chen et al., 2013, Saunders et al., 2015, Bressler et al., 2017). By contrast, exposure to loud noises typically does not rupture the tympanic membrane, meaning that mechanical over-stimulation of the inner ear can be sustained, potentially resulting in more long-term hearing loss (Yang et al., 2011). Therefore, damage to hair cells, spiral ganglion neurons, and the central auditory pathway resulting from these distinctly different auditory traumas may vary greatly (Luo et al., 2014a, Luo et al., 2014b, Niwa et al., 2016, Luo et al., 2017).

In addition to hearing loss, blasts cause traumatic brain injury (TBI) and may introduce additional pathologies to the central auditory pathway (Kamnaksh et al., 2011, Mao et al., 2012, Valiyaveettil et al., 2012, Tate et al., 2014, Race et al., 2017). Solid body structures, such as the brain, were previously considered to be at low-risk of sustaining shockwave injury (Argyros, 1997, Elsayed, 1997, Stuhmiller, 1997, Cernak et al., 2001). However, subsequent studies have revealed a wide range of cellular injuries and inflammatory responses that occur despite a lack of hemorrhage or gross brain damage (Cernak et al., 2001, Sajja et al., 2012, Abdul-Muneer et al., 2013, Arun et al., 2013). For example, shockwaves from a single blast can compromise the membranes of neural and glial cells, allowing intracellular proteins to leak into cerebrospinal fluid (Saljo et al., 2003, Leung et al., 2008). Likewise, shockwave exposure activates resident microglia and astrocytes within 30 min (Kaur et al., 1995, Cernak et al., 2001, Cernak et al., 2011, Saljo et al., 2001, Svetlov et al., 2010, Du et al., 2017). Activated microglia subsequently release TNF-α and other pro-inflammatory cytokines, generating both acute and chronic cellular inflammatory responses (Garden and Moller, 2006).

Here we examine the effects of blast shockwave exposure on the auditory frequency map in the primary auditory cortex (AI) of the rat. We found that blast exposure resulted in distorted frequency maps with over-representation of seemingly random narrow frequency ranges.

Section snippets

Animals

All procedures used in this study were approved by the Animal Care and Use Committees at the University of Arizona and Wayne State University. Ten Sprague–Daley rats, male and 2-month-old, were purchased from Charles River and used in this study. Five were chosen randomly and assigned to the blast-exposed group and the remaining five rats were assigned to the sham-exposed group.

Blast exposure and behavioral tests

Blast exposure was performed as described before (Mao et al., 2012). The rat was anesthetized with isoflurane (0.75–1%

Results

The cortical frequency map in AI was examined in blast- and sham-exposed animals 3 months after the exposure. AI frequency maps of sham-exposed animals were tonotopically organized, with all frequencies approximately equally represented in each animal (one-sample Kolmogorov–Smirnov’s test against a log-uniform distribution from 2 kHz to 32 kHz, p > 0.1; for example, see Fig. 1, Z-3 and Z-14). By contrast, all blast-exposed animals had a large area in AI that over-represented a relatively narrow

Discussion

In this study we have shown that blast exposure disrupts the AI frequency map and changes neuronal response properties. Some of these changes are similar to those observed in animals following noise exposure. For example, the increased response threshold and shortened response latencies observed in this study have previously been reported following noise exposure (Gallo and Glorig, 1964, Syka and Rybalko, 2000, Norena et al., 2003). Noise exposure often results in hearing loss in a limited

Acknowledgment

The research was supported by Department of Defense (W81XWH-11-2-0031). We thank Alexander K. Zinsmaier for comments on the manuscript.

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