Noise trauma induced plastic changes in brain regions outside the classical auditory pathway
Graphical abstract
Introduction
Intense noise exposures have long been known to induce temporary or permanent noise-induced hearing loss (NIHL) and cochlear damage that reduces neural output of the cochlea. Paradoxically, NIHL often results in enhanced sound-evoked responses in the central auditory pathway indicative of enhanced central gain, a form of homeostatic plasticity that partially compensates or overcompensates for peripheral hearing loss (Salvi et al., 1990, Salvi et al., 2000, Syka and Rybalko, 2000, Popelar et al., 2008, Sun et al., 2008). The enhanced sound-evoked activity observed in central auditory structures is often greatest at frequencies below the region of NIHL possibly due to a reduction in lateral inhibition (Salvi et al., 2000). In addition to changes in central gain, NIHL typically results in an increase in spontaneous discharge rates (SRs) in the cochlear nucleus (CN) which in some cases continues rostral up to the auditory cortex (AC) (Eggermont and Komiya, 2000, Kaltenbach and Afman, 2000, Zhang et al., 2006, Dong et al., 2010, Mulders and Robertson, 2013, Luo et al., 2014). Enhanced sound-evoked responses and increased central gain have been linked to hyperacusis or loudness intolerance (Sun et al., 2012) whereas elevated SR in tonotopic regions associated with hearing loss is considered by some as the neural correlate of tinnitus (Chen and Jastreboff, 1995, Kaltenbach and Afman, 2000). NIHL also induces frequency map reorganization in the AC and enhanced inter-neuronal synchrony; these neurophysiological changes have also been linked to tinnitus (Muhlnickel et al., 1998, Seki and Eggermont, 2002, Eggermont, 2006, Norena and Eggermont, 2006).
NIHL also exerts effects beyond the classical auditory pathway. NIHL suppresses neurogenesis in the hippocampus and alters the spatial tuning of hippocampal neurons as animals navigate through a maze (Goble et al., 2009, Kraus et al., 2010, Newman et al., 2015). The amygdala, which attaches emotional significance to sounds, plays a central role in auditory fear conditioning and modulates the acoustic startle reflex (LeDoux, 2000, Kraus and Canlon, 2012). In this context, it is interesting to note that the amplitude of acoustic startle reflex is greatly depressed by unilateral NIHL. Since unilateral ear plugging also suppresses startle reflex amplitude, it seems likely that the sensory or motor circuits that regulate the startle reflex requires information from both ears (Kraus et al., 2010, Lobarinas et al., 2013). The Str, which is involved in motor planning and movements, receives auditory inputs and can modulate the startle reflex (Bordi and LeDoux, 1992, Kodsi and Swerdlow, 1995). Sound-evoked neural activity in the Str is also greatly enhanced by sodium salicylate, an ototoxic drug that induces tinnitus and hyperacusis (Chen et al., 2014b). Although the neural correlates of tinnitus and hyperacusis have been extensively studied in the classical auditory pathway, there is growing awareness that non-classical auditory areas such as the amygdala and Str may contribute directly or indirectly to these aberrant perceptions (Jastreboff, 2007, Rauschecker et al., 2010, Chen et al., 2012). Some clinical reports suggest that the amygdala and Str are involved in tinnitus and hyperacusis (De Ridder et al., 2006, Cheung and Larson, 2010). The lateral amygdala (LA) and striatum (Str) have extensive connections with the classical auditory pathway (Romanski et al., 1993, Budinger et al., 2008) and respond robustly to acoustic stimulation (Bordi et al., 1993, Romanski et al., 1993, Quirk et al., 1995, Cromwell et al., 2007, Chen et al., 2012). Therefore the response properties of neurons in the LA and Str are likely to be altered by NIHL. Although the effects of acoustic trauma have been explored at many different sites in the classical auditory pathways, the effects of NIHL on non-classical auditory centers are poorly understood. To address this issue, we studied the effects of high-frequency NIHL on the sound-evoked responses and SR in the LA and Str of the rat and compared the results to similar data obtained from primary and secondary AC.
Section snippets
Subjects
Sprague–Dawley rats (2 months of age) were acquired from Charles River Laboratories Inc. (Wilmington, MA, USA) and housed in the Laboratory Animal Facility (LAF) of the University at Buffalo and given free access to food and water. The colony room was maintained at 22 °C with a 12-h light–dark cycle. All procedures regarding the use and handling of animals were reviewed and approved by the Institutional Animal Care and Use Committee (IACUC) at the University at Buffalo.
Noise exposure
NIHL was induced with
ABR threshold shift and hair cell loss
Fig. 2A shows the magnitudes of ABR threshold shifts of four rats as a function of frequency caused by the 10–20-kHz OBN (104-dB SPL for 35 days). The exposure caused a mean PTS of 20–40 dB between 12 and 32 kHz, but had little or no effect at 4 and 8 kHz. The mean PTS in the noise band (12–20 kHz) was ∼33 dB. Fig. 2B shows percent OHC and IHC loss of the four rats as a function of percent distance from the apex of the cochlea; cochlear location is related to frequency on the upper x-axis (Muller, 1991
Discussion
Noise-induced hearing loss reduces the neural output of the cochlea leading to unexpected functional changes in the central auditory pathway such as tonotopic map reorganization in AC and medial geniculate body (Willott et al., 1993, Eggermont and Komiya, 2000, Kamke et al., 2003), loss of surround inhibition in AC, (Rajan, 1998), suprathreshold sound-evoked hyperactivity in the inferior colliculus (IC) and higher auditory centers (Salvi et al., 1990, Syka, 2002) and increased SR in the dorsal
Acknowledgements
This work was supported in part by grants from the National Institutes of Health (R01DC009219, 5R01DC011808) and ONR (N000141210731). The authors declare no competing financial interests or conflicts of interest.
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