Noise Overexposure Alters Long-Term Somatosensory-Auditory Processing in the Dorsal Cochlear Nucleus-Possible Basis for Tinnitus-Related Hyperactivity?

Kresge Hearing Research Institute, University of Michigan, Ann Arbor, Michigan 48109, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 02/2012; 32(5):1660-71. DOI: 10.1523/JNEUROSCI.4608-11.2012
Source: PubMed


The dorsal cochlear nucleus (DCN) is the first neural site of bimodal auditory-somatosensory integration. Previous studies have shown that stimulation of somatosensory pathways results in immediate suppression or enhancement of subsequent acoustically evoked discharges. In the unimpaired auditory system suppression predominates. However, damage to the auditory input pathway leads to enhancement of excitatory somatosensory inputs to the cochlear nucleus, changing their effects on DCN neurons (Shore et al., 2008; Zeng et al., 2009). Given the well described connection between the somatosensory system and tinnitus in patients we sought to determine whether plastic changes in long-lasting bimodal somatosensory-auditory processing accompany tinnitus. Here we demonstrate for the first time in vivo long-term effects of somatosensory inputs on acoustically evoked discharges of DCN neurons in guinea pigs. The effects of trigeminal nucleus stimulation are compared between normal-hearing animals and animals overexposed with narrow band noise and behaviorally tested for tinnitus. The noise exposure resulted in a temporary threshold shift in auditory brainstem responses but a persistent increase in spontaneous and sound-evoked DCN unit firing rates and increased steepness of rate-level functions. Rate increases were especially prominent in buildup units. The long-term somatosensory enhancement of sound-evoked responses was strengthened while suppressive effects diminished in noise-exposed animals, especially those that developed tinnitus. Damage to the auditory nerve is postulated to trigger compensatory long-term synaptic plasticity of somatosensory inputs that might be an important underlying mechanism for tinnitus generation.

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    • "Interestingly, similar to the long-term changes in firing activity of fusiform cells, auditory-Sp5 bimodal stimulation induced persistent changes in the tone and RLF responses of primary-like cells in VCN (Figs. 5A and B) but not in the IC (Figs. 5C and D). The long-term effects correspond to the upregulation of somatosensory innervation in CN (Section 4.3), and likely underlie induction of hyperactivity and tinnitus (Dehmel et al., 2012). Indeed, as IC does not exhibit long-term bimodal plasticity, a probable induction mechanism (Fig. 5D), IC hyperactivity probably cannot occur independently of DCN hyperactivity ( "
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    • "glutamatergic drive from non-auditory structures, as well as synaptic plasticity, alters these interactions to produce enhancement of neural activity (Dehmel et al. 2012; Koehler and Shore 2013). The mechanisms by which the CN adaptively filters auditory signals are also altered following noise overexposure and tinnitus: the timing rules that demonstrate this integration are inverted (Hebbian to anti-Hebbian) and are broadened in animals showing behavioral signs of tinnitus (Koehler and Shore 2013). "
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    • "ncement of somatosensory input into the DCN driven by traumatic threshold elevations has been described ( Shore et al . , 2008 ) . This modified sensory afferent input in the DCN is accompanied by alterations of the typical stimulus timing - dependent plasticity rules for bimodal integration during successive auditory / somatosensory stimulation ( Dehmel et al . , 2012b ; Koehler and Shore , 2013a , b ) ( Figure 6 ) , generally producing a long - term enhancement of uni - modal acoustically evoked activity . Given that earlier descriptions of the effects of cochlear trauma concluded the absence of plas - tic remapping in the DCN ( Kaltenbach et al . , 1992 ; Rajan and Irvine , 1998 ) , it is worthwhile"
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