Research paperDevelopment of hyperactivity after acoustic trauma in the guinea pig inferior colliculus
Highlights
► Spontaneous firing in inferior colliculus at varying times after acoustic trauma. ► Elevated firing rates (hyperactivity) appear between 4 and 12 h post trauma. ► Hyperactivity becomes more restricted in frequency region over time.
Introduction
Acoustic trauma is known in animal models to result in increased spontaneous activity (so-called hyperactivity), in a sub-population of neurons in central auditory structures such as the cochlear nucleus (CN), inferior colliculus (IC) and auditory cortex (AC) (Brozoski et al., 2002; Dong et al., 2010; Kaltenbach et al., 2000; Komiya and Eggermont, 2000; Mulders and Robertson, 2009, 2011; Norena and Eggermont, 2003; Seki and Eggermont, 2003). This hyperactivity has been suggested as a possible neural substrate for tinnitus, a phantom hearing sensation frequently associated with cochlear trauma (Bauer et al., 2008; Brozoski et al., 2002; Kaltenbach et al., 2004).
Surprisingly, the detailed time course of the onset of hyperactivity after cochlear trauma has received little systematic attention. In the AC of cats, Seki and Eggermont (2003) reported increased single unit spontaneous rates 1 week after loud sound exposure. In a similar preparation, Norena and Eggermont (2003) used spike sorting of cortical multiunit clusters and reported that spontaneous firing rates were not immediately altered but increased above pre-exposure levels “a few hours” post trauma. Single unit recordings in guinea pig IC and ventral cochlear nucleus (VCN), found hyperactivity 1 and 2 weeks post trauma respectively (Mulders and Robertson, 2009, 2011; Robertson et al., 2013). Mulders and Robertson (2009) reported no significant hyperactivity in guinea pig IC immediately after acoustic trauma (0–4 h post-trauma) but other recovery times shorter than 1 week were not investigated. In the dorsal cochlear nucleus (DCN) of hamsters, multiunit activity was reported to be reduced 2 days post-exposure and elevated between 2 and 5 days post trauma (Kaltenbach et al., 2000). In the IC of the same species, multiunit activity was elevated 7 days post-exposure (Manzoor et al., 2013), but shorter recovery times were not investigated.
In addition to differences in species, anaesthetic regimes, site of recording and recovery times, any comparison between these studies is further confounded by the fact that a range of acoustic trauma parameters was employed.
Hence the present study was undertaken to provide more complete data on the time of onset of hyperactivity in IC, in the one species, using a fixed acoustic trauma regime.
Section snippets
Animals
Twenty four adult pigmented guinea pigs of either sex, weighing between 260 and 385 g at the time of initial anaesthesia were included in this study. The experimental protocols conformed to the Code of Practice of the National Health and Medical Research Council of Australia, and were approved by the Animal Ethics Committee of The University of Western Australia.
Surgical procedures
Details of all procedures have been presented in previous publications (Mulders and Robertson, 2009, 2011; Robertson et al., 2013;
Peripheral thresholds
As reported previously, the acoustic trauma resulted in immediate changes in CAP thresholds, followed by progressive but partial recovery of threshold. As shown in Fig. 1, immediately after exposure CAP thresholds were markedly elevated for sound frequencies from 8 to 24 kHz, but as recovery time increased, the range of frequencies over which the CAP thresholds remained elevated became mainly confined to frequencies above 10 kHz and the maximum CAP threshold loss also reduced in magnitude. This
Discussion
The present results are consistent with the view that hyperactivity in the guinea pig IC begins to develop some time between about 4 h and 12 h post-acoustic trauma. This is the first systematic study of the timing of onset of hyperactivity in the auditory midbrain and it shows that although hyperactivity is not an immediate consequence of the peripheral trauma, for instance due to a loss of inhibitory side-bands, it is nonetheless a relatively rapid plastic phenomenon, appearing within hours
Acknowledgements
Supported by grants from Action on Hearing Loss (UK), the Medical Health and Research Infrastructure Fund (WA), the Neurotrauma Research Program and the University of Western Australia. The authors are grateful to an anonymous referee of an earlier paper for raising the central issue addressed in this work.
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