Elsevier

Neuroscience

Volume 315, 19 February 2016, Pages 228-245
Neuroscience

Noise trauma induced plastic changes in brain regions outside the classical auditory pathway

https://doi.org/10.1016/j.neuroscience.2015.12.005Get rights and content

Highlights

  • High-frequency noise trauma induces hypoactivity at high-frequencies but hyperactivity at low-frequencies.

  • A severe injury induces hypoactivity not only at the high-frequencies but also at the edge-frequency.

  • A moderate injury induces hypoactivity at the high-frequencies but not at the edge-frequency.

  • A minor injury, in contrast, induces hyperactivity at the edge-frequency but not at the low-frequency.

  • The noise-induced hyperactivity occurs in the auditory cortex and lateral amygdala but not in striatum.

Abstract

The effects of intense noise exposure on the classical auditory pathway have been extensively investigated; however, little is known about the effects of noise-induced hearing loss on non-classical auditory areas in the brain such as the lateral amygdala (LA) and striatum (Str). To address this issue, we compared the noise-induced changes in spontaneous and tone-evoked responses from multiunit clusters (MUC) in the LA and Str with those seen in auditory cortex (AC) in rats. High-frequency octave band noise (10–20 kHz) and narrow band noise (16–20 kHz) induced permanent threshold shifts at high-frequencies within and above the noise band but not at low frequencies. While the noise trauma significantly elevated spontaneous discharge rate (SR) in the AC, SRs in the LA and Str were only slightly increased across all frequencies. The high-frequency noise trauma affected tone-evoked firing rates in frequency and time-dependent manner and the changes appeared to be related to the severity of noise trauma. In the LA, tone-evoked firing rates were reduced at the high-frequencies (trauma area) whereas firing rates were enhanced at the low-frequencies or at the edge-frequency dependent on severity of hearing loss at the high frequencies. The firing rate temporal profile changed from a broad plateau to one sharp, delayed peak. In the AC, tone-evoked firing rates were depressed at high frequencies and enhanced at the low frequencies while the firing rate temporal profiles became substantially broader. In contrast, firing rates in the Str were generally decreased and firing rate temporal profiles become more phasic and less prolonged. The altered firing rate and pattern at low frequencies induced by high-frequency hearing loss could have perceptual consequences. The tone-evoked hyperactivity in low-frequency MUC could manifest as hyperacusis whereas the discharge pattern changes could affect temporal resolution and integration.

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.

References (106)

  • T.J. Goble et al.

    Acute high-intensity sound exposure alters responses of place cells in hippocampus

    Hear Res

    (2009)
  • L.M. Grant et al.

    Relationships among rat ultrasonic vocalizations, behavioral measures of striatal dopamine loss, and striatal tyrosine hydroxylase immunoreactivity at acute and chronic time points following unilateral 6-hydroxydopamine-induced dopamine depletion

    Behav Brain Res

    (2015)
  • L. Hu et al.

    Chronic scream sound exposure alters memory and monoamine levels in female rat brain

    Physiol Behav

    (2014)
  • P.J. Jastreboff

    Tinnitus retraining therapy

    Prog Brain Res

    (2007)
  • J.A. Kaltenbach et al.

    Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus

    Hear Res

    (2000)
  • J.A. Kaltenbach et al.

    Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure

    Hear Res

    (2000)
  • M. Knipper et al.

    Advances in the neurobiology of hearing disorders: recent developments regarding the basis of tinnitus and hyperacusis

    Prog Neurobiol

    (2013)
  • K.S. Kraus et al.

    Neuronal connectivity and interactions between the auditory and limbic systems. Effects of noise and tinnitus

    Hear Res

    (2012)
  • K.S. Kraus et al.

    Noise trauma impairs neurogenesis in the rat hippocampus

    Neuroscience

    (2010)
  • G.S. Lee et al.

    Effects of hearing aid amplification on voice F0 variability in speakers with prelingual hearing loss

    Hear Res

    (2013)
  • B.J. Liddell et al.

    A direct brainstem-amygdala-cortical ’alarm’ system for subliminal signals of fear

    NeuroImage

    (2005)
  • E. Lobarinas et al.

    The gap-startle paradigm for tinnitus screening in animal models: limitations and optimization

    Hear Res

    (2013)
  • J.C. Milbrandt et al.

    GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma

    Hear Res

    (2000)
  • W.H. Mulders et al.

    Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus

    Hear Res

    (2013)
  • M. Muller

    Frequency representation in the rat cochlea

    Hear Res

    (1991)
  • K. Muramoto et al.

    Rat amygdaloid neuron responses during auditory discrimination

    Neuroscience

    (1993)
  • A.J. Newman et al.

    Low-cost blast wave generator for studies of hearing loss and brain injury: blast wave effects in closed spaces

    J Neurosci Methods

    (2015)
  • J. Popelar et al.

    Comparison of noise-induced changes of auditory brainstem and middle latency response amplitudes in rats

    Hear Res

    (2008)
  • J. Popelar et al.

    Effect of noise on auditory evoked responses in awake guinea pigs

    Hear Res

    (1987)
  • C. Qiu et al.

    Inner hair cell loss leads to enhanced response amplitudes in auditory cortex of unanesthetized chinchillas: evidence for increased system gain

    Hear Res

    (2000)
  • G.J. Quirk et al.

    Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat

    Neuron

    (1995)
  • J.P. Rauschecker et al.

    Tuning out the noise: limbic-auditory interactions in tinnitus

    Neuron

    (2010)
  • D. Robertson et al.

    Spontaneous hyperactivity in the auditory midbrain: relationship to afferent input

    Hear Res

    (2013)
  • R. Salvi et al.

    Single auditory nerve fiber and action potential latencies in normal and noise-treated chinchilla

    Hear Res

    (1979)
  • R.J. Salvi et al.

    Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma

    Hear Res

    (1990)
  • R.J. Salvi et al.

    Auditory plasticity and hyperactivity following cochlear damage

    Hear Res

    (2000)
  • S. Seki et al.

    Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss

    Hear Res

    (2002)
  • S. Seki et al.

    Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss

    Hear Res

    (2003)
  • S.H. Sha et al.

    Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals

    Hear Res

    (2001)
  • D. Stolzberg et al.

    Salicylate-induced peripheral auditory changes and tonotopic reorganization of auditory cortex

    Neuroscience

    (2011)
  • W. Sun et al.

    Noise exposure enhances auditory cortex responses related to hyperacusis behavior

    Brain Res

    (2012)
  • W. Sun et al.

    Noise exposure-induced enhancement of auditory cortex response and changes in gene expression

    Neuroscience

    (2008)
  • J. Syka et al.

    Threshold shifts and enhancement of cortical evoked responses after noise exposure in rats

    Hear Res

    (2000)
  • J. Wang et al.

    Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage

    Hear Res

    (2002)
  • J. Wang et al.

    Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons

    Brain Res

    (2002)
  • D. Algom et al.

    Binaural and temporal integration of the loudness of tones and noises

    Percept Psychophys

    (1989)
  • A.K. Anweiler et al.

    Spectral loudness summation for short and long signals as a function of level

    J Acoust Soc Am

    (2006)
  • G.R. Atherley et al.

    Study of tinnitus induced temporarily by noise

    J Acoust Soc Am

    (1968)
  • B.D. Auerbach et al.

    Central gain control in tinnitus and hyperacusis

    Front Neurol

    (2014)
  • F. Bordi et al.

    Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum

    J Neurosci

    (1992)
  • Cited by (35)

    • Prenatal stress dysregulates resting-state functional connectivity and sensory motifs

      2021, Neurobiology of Stress
      Citation Excerpt :

      The auditory system connects to the autonomic nervous system (ANS) (including brain mechanisms underlying, stress, arousal, startle, and blood pressure) via the amygdala and other circuits (Burow et al., 2005; Eggermont, 2014; Jafari et al., 2020b). Thus, noise can activate non-classical auditory-responsive brain areas, trigger the emotion/fear system of the brain (Chen et al., 2016; Eggermont, 2014), and lead to the release of stress-related hormones, including corticotropin-releasing hormone (CRH), corticosterone, and norepinephrine (Burow et al., 2005; Eggermont, 2014). Considering the connection between the auditory system and the neural system underlying stress signaling, cortical auditory responses might show more susceptibility to noise stress than other sensory responses.

    View all citing articles on Scopus
    View full text