Elsevier

Hearing Research

Volume 183, Issues 1–2, September 2003, Pages 137-153
Hearing Research

Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus

https://doi.org/10.1016/S0378-5955(03)00225-9Get rights and content

Abstract

Changes in spontaneous activity, recorded over 15-min periods before, immediately after and within hours after an acute acoustic trauma, were studied in primary auditory cortex of ketamine-anesthetized cats. We focused on the spontaneous firing rate (SFR), the peak cross-correlation coefficient (ρ) and burst-firing activity. Multi-units (MUs) were grouped according to characteristic frequency (CF): MUs with a CF below the trauma-tone frequency (TF) were labeled as Be, those with a CF within 1 octave above the TF were labeled as Ab1 and those with a CF more than 1 octave above the TF were labeled as Ab2. Immediately after the trauma, the SFR was not significantly changed. The percentage of time that neurons were bursting, the mean burst duration, the number of spikes per burst and the mean inter-spike interval in a burst were enhanced. ρ was locally increased in the Ab1-Ab2 and Ab2-Ab2 groups. A few hours post trauma, the SFR was increased in the Be and Ab2 groups, whereas burst-firing returned to pre-exposure levels. Moreover, ρ was elevated in the Be-Ab2, Ab1-Ab2 and Ab2-Ab2 groups; this increase was significantly correlated to the changes in SFR. The results are discussed in the context of a neural correlate of tinnitus.

Introduction

Tinnitus is a phantom sound (e.g., ringing, hissing or whistling) sensation perceived without any physical stimulation. This symptom is prevalent among about 10% of the general population and alters significantly the quality of life of patients experiencing it. Consequently, a large number of studies (reviewed in Møller, 1984, Jastreboff, 1990, Eggermont, 2000, Kaltenbach, 2000, Baguley, 2002) have been conducted over the last two decades to provide the necessary insight into the potential neurophysiological mechanisms of tinnitus. A better understanding of the origins of tinnitus is a prerequisite for successful therapeutic avenues. Moreover, explaining tinnitus requires identifying neural signals that induce a ‘phantom’ perception, and allow auditory perception in general to be linked with neural coding.

Tinnitus is likely related to aberrant neural activity generated at a given level in the auditory system (Eggermont, 1990b, Jastreboff, 1990). There is, however, no consensus on the level in the auditory system at which this signal is generated, or on the nature of the abnormal signal underlying tinnitus. Some authors have suggested that the abnormal signal may be generated at the peripheral level (Jastreboff, 1990, Eggermont, 1990b, Martin et al., 1993, Cazals et al., 1998, Puel et al., 2002, Guitton et al., 2003), whereas others have proposed a central generation – beyond the auditory nerve level (Gerken, 1996, Eggermont and Kenmochi, 1998, Salvi et al., 2000, Eggermont and Komiya, 2000, Kaltenbach and McCaslin, 1996, Kaltenbach and Afman, 2000, Zacharek et al., 2002, Brozoski et al., 2002, Noreña et al., 2000, Noreña et al., 2002a, Noreña et al., 2002b, Noreña and Eggermont, 2003). Moreover, the nature of the aberrant neural signal is still a matter of debate. Some have proposed that tinnitus may be related to an increase in spontaneous firing rate (SFR) (Tonndorf, 1987, Jastreboff et al., 1988, Jastreboff, 1990, Chen and Jastreboff, 1995, Gerken, 1996, Eggermont and Komiya, 2000, Kaltenbach and McCaslin, 1996, Kaltenbach and Afman, 2000, Brozoski et al., 2002, Zacharek et al., 2002). Others have suggested that changes in the temporal pattern of spontaneous discharges may be associated with tinnitus. In this context, it has been proposed that aberrant perceptions such as tinnitus (or even chronic pain) may be related to an increased spontaneous burst-firing activity in the auditory system (Eggermont, 1984, Eggermont, 1990b, Møller, 1984, Puel, 1995, Chen and Jastreboff, 1995, Jeanmonod et al., 1996). The assumption is the following: if the inter-spike interval (ISI) within the burst is shorter than the time constant for integration of excitatory inputs of a target cell, the excitatory postsynaptic potentials (EPSPs) will summate thereby increasing the probability of firing in the postsynaptic cell. Moreover, even sub-threshold EPSPs will be able to elicit spiking in the target cell. Finally, an enhanced synchrony between discharges at auditory nerve (Eggermont, 1984, Eggermont, 1990b, Møller, 1984, Martin et al., 1993, Cazals et al., 1998) or cortical levels (Ochi and Eggermont, 1996, Ochi and Eggermont, 1997) has been suggested to cause tinnitus. An enhanced synchrony of inputs is another way to increase the probability of making a target cell fire (Abeles, 1991).

In addition, changes in the tonotopic organization of the auditory cortex have been suggested as a neural correlate of tinnitus (Muhlnickel et al., 1998, Rauschecker, 1999, Noreña et al., 2002a, Noreña et al., 2002b).

A treatment known to induce tinnitus in humans is assumed to induce tinnitus in animals or to reveal at least the peripheral and/or central changes potentially involved in the emergence of tinnitus. In this context, the effects of various tinnitus-inducing agents such as salicylate, quinine and acute or chronic noise trauma have provided numerous potential correlates of tinnitus in animals. Chen and Jastreboff (1995) showed a dramatic change in burst-firing (increase in the number of spikes within a burst) in inferior colliculus (IC) after salicylate administration. Furthermore, a calcium supplement in drinking water, at a dose known to prevent the emergence of tinnitus (Jastreboff and Sasaki, 1994), abolishes the changes in bursting activity. Eggermont and Kenmochi (1998) found an increase in SFR in secondary auditory cortex (AII) after salicylate or quinine injection. Moreover, it has been found that quinine increased the synchrony between simultaneously recorded neurons in primary auditory cortex (AI) (Ochi and Eggermont, 1997). It has been shown that a chronic acoustic trauma or cisplatin induced an increase in SFR in the dorsal cochlear nucleus (DCN) (Zhang and Kaltenbach, 1998, Kaltenbach and Afman, 2000, Kaltenbach et al., 2002, Rachel et al., 2002). Finally, an increase in SFR has been noticed in AI after acute (Kimura and Eggermont, 1999) and chronic acoustic trauma (Eggermont and Komiya, 2000, Seki and Eggermont, 2003). A current challenge is to unify the various neural correlates found across studies. Specifically, the relevance of the central changes induced by tinnitus-inducing agents (as actual neural correlates of tinnitus) needs to be addressed. Furthermore, it is important to know whether one or multiple mechanisms can lead to tinnitus, e.g., does salicylate-induced tinnitus share similar mechanisms with acoustic trauma-induced tinnitus?

In humans, an acute acoustic trauma is generally immediately followed by tinnitus (Loeb and Smith, 1967, Chermak and Dengerink, 1987, Temmel et al., 1999, Metternich and Brusis, 1999, Stankiewicz et al., 2000, Mrena et al., 2002). Interestingly, the conditions of exposure (duration, intensity and spectrum of the trauma stimulus) do not significantly affect the induction of tinnitus. For example, conditions as different as firearm shooting (Mrena et al., 2002, Temmel et al., 1999), car airbag release (Stankiewicz et al., 2000), minutes of exposure to tones or noise (Loeb and Smith, 1967, Chermak and Dengerink, 1987) and hours of exposure to recreational music (Metternich and Brusis, 1999) have been reported to immediately cause tinnitus.

The goal of the present study was to further elucidate potential electrophysiological correlates of acoustic trauma-induced tinnitus. Here, we report the immediate effects of an acoustic trauma (exposure to a 5- or 6-kHz pure tone at about 120 dB SPL for 1 h) on the pattern of spontaneous activity (SA) of neurons in AI recorded with multi-electrode arrays. The SFR and the peak cross-correlation coefficient (ρ) were assessed before and after the trauma. In addition, the effects of the trauma on burst-firing activity were also addressed.

Moreover, the pitch of tinnitus induced after a 5-min exposure to 90 dB SPL pure tones is positively correlated with the tone frequency. The frequency of the maximum hearing loss was located at about 0.7 octave above the trauma frequency, whereas tinnitus pitch was found to be higher, namely at about 1 octave above the trauma frequency (Loeb and Smith, 1967). Consequently, changes in neural activity potentially related to tinnitus are expected immediately after the trauma, and within the frequency band located at around 1 octave above the trauma-tone frequency (TF).

Our previous studies focused on the chronic (Seki and Eggermont, 2003) or acute effects of a noise trauma on SFR (Kimura and Eggermont, 1999). Importantly, the latter study (Kimura and Eggermont, 1999) addressed the effects of a noise trauma on neurons with a characteristic frequency (CF) below the trauma frequency – namely, on neurons that we do not expect to be involved in the generation of tinnitus. In the present study, multi-units (MUs) with a CF below and above the TF were recorded.

Section snippets

Methods

The care and the use of animals reported in this study was approved (#BI 2001-021) by the Life and Environmental Sciences Animal Care Committee of the University of Calgary. All animals were maintained and handled according to the guidelines set by the Canadian Council of Animal Care.

Results

Recordings were made from the right AI in 16 cats. The ages of the cats were from 90 days to 202 days (mean=154 days, S.D.=30.8 days). We recorded neural activity continuously from 124 MU clusters several hours before and up to 6 h after the pure tone trauma. The study presented here includes data collected in conjunction with a companion study (Noreña et al., 2003). The latter study focused on the changes in frequency-tuning properties and driven discharges of MUs after an acute acoustic

Discussion

The results of the present study can be summarized as follows. First, the trauma induced a shift in the response area of MUs, with the emergence of new responses. Specifically, a significant shift of CF toward the TF was noticed in the Ab2 group (Fig. 2, Fig. 3). These results have been fully described in a companion paper (Noreña et al., 2003) and they will only be discussed briefly in the present one. Moreover, the acoustic trauma induced significant changes in the pattern of SA. Immediately

Acknowledgements

This work was supported by the Alberta Heritage Foundation for Medical Research, the National Sciences and Engineering Research Council, a CIHR-NET grant, the American Tinnitus Association, the Canadian Language and Literacy Research Network, and the Campbell McLaurin Chair for Hearing Deficiencies.

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