Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates 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.
References (95)
- et al.
Rapid changes in the frequency tuning of neurons in cat auditory cortex resulting from pure-tone-induced temporary threshold shift
Neuroscience
(1993) - et al.
Salicylate-induced abnormal activity in the inferior colliculus of rats
Hear. Res.
(1995) On the pathophysiology of tinnitus; a review and a peripheral model
Hear. Res.
(1990)- et al.
Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex
Hear. Res.
(1998) - et al.
Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood
Hear. Res.
(2000) - et al.
Ultrastructural studies of stereocilia in noise-exposed rabbits
Hear. Res.
(1983) Central tinnitus and lateral inhibition: an auditory brainstem model
Hear. Res.
(1996)Phantom auditory perception (tinnitus): mechanisms of generation and perception
Neurosci. Res.
(1990)- 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) - et al.
Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure
Hear. Res.
(2000)
Effects of acute pure tone induced hearing loss on response properties in three auditory cortical fields in cat
Hear. Res.
Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates
Hear. Res.
Acute ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates
Hear. Res.
GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma
Hear. Res.
Comparison between local field potentials and unit cluster activity in primary auditory cortex and anterior auditory field in the cat
Hear. Res.
An auditory negative after-image as a human model of tinnitus
Hear. Res.
Effects of salicylate on neural activity in cat primary auditory cortex
Hear. Res.
Effects of quinine on neural activity in cat primary auditory cortex
Hear. Res.
Short-term plasticity of the human auditory cortex
Brain Res.
Chemical synaptic transmission in the cochlea
Prog. Neurobiol.
Inner hair cell loss leads to enhanced response amplitudes in auditory cortex of unanesthetized chinchillas: evidence for increased system gain
Hear. Res.
Increases in spontaneous neural activity in the hamster dorsal cochlear nucleus following cisplatin treatment: a possible basis for cisplatin-induced tinnitus
Hear. Res.
Auditory cortical plasticity: a comparison with other sensory systems
Trends Neurosci.
Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea
Hear. Res.
Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea
Hear. Res.
Auditory Plasticity and hyperactivity following cochlear damage
Hear. Res.
Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss
Hear. Res.
The analogy between tinnitus and pain: a suggestion for a physiological basis of chronic tinnitus
Hear. Res.
Responses from the AVCN units in the cat before and after inducement of an acute noise trauma
Hear. Res.
Interocular transfer of receptive field expansion in cat visual cortex
Vis. Res.
Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons
Brain Res.
Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound
Neurosci. Lett.
Artifactual synchrony via capacitance coupling in multi-electrode recording from cat striate cortex
J. Neurosci. Methods
Mechanisms of tinnitus
Br. Med. Bull.
Correlations without synchrony
Neural Comput.
Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex
Eur. J. Neurosci.
Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus
J. Neurosci.
Alterations in average spectrum of cochleoneural activity by long-term salicylate treatment in the guinea pig: a plausible index of tinnitus
J. Neurophysiol.
Characteristics of temporary noise-induced tinnitus in male and female subjects
Scand. Audiol.
Properties of auditory nerve responses in absence of outer hair cells
J. Neurophysiol.
Receptive field expansion in adult visual cortex is linked to dynamic changes in strength of cortical connections
J. Neurophysiol.
Primary cortical representation of sounds by the coordination of action-potential timing
Nature
Involvement of N-methyl-D-asparte receptors in epileptiform bursting in the rat hippocampal slice
J. Physiol.
Alterations in correlated activity parallel ICMS-induced representational plasticity
NeuroReport
Cited by (401)
Comparing tinnitus, pain, psychosocial and cognitive factors between patients with tinnitus and pain: A systematic review
2023, Journal of Psychosomatic ResearchAcoustic deprivation modulates central gain in human auditory brainstem and cortex
2023, Hearing ResearchCitation Excerpt :The functional consequence of homeostatic plasticity is a change (increase or decrease) in the potentiation of neural activity in the central pathway, referred to as “central gain,” and often described as “an internal volume control” (e.g., Brotherton et al., 2015). Physiological evidence of central gain modulation in the auditory system has been shown in animal models following cochlear damage as increased spontaneous activity in the cochlear nucleus and inferior colliculus (e.g., Kaltenbach et al., 2002; Manzoor et al., 2013), and auditory cortex (e.g., Noreña and Eggermont, 2003), and as enhanced stimulus-driven activity in the central pathway and cortex (e.g., Chambers et al., 2016; Hickox and Liberman, 2014; Salvi et al., 2000). While an internal volume control seems appealing in the case of hearing loss, excessive central gain of spontaneous activity, as well as potential contributions from stochastic resonance, may partially explain the perception of tinnitus (Hébert et al., 2013; Noreña, 2011; Noreña and Farley, 2013; Schaette and Kempter, 2008, 2006; Schaette and McAlpine, 2011; Schilling et al., 2021) and reduced sound tolerance in the case of hyperacusis (Gu et al., 2010; Knudson et al., 2014; Noreña and Farley, 2013).