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REVIEW ARTICLE Table of Contents   
Year : 1999  |  Volume : 1  |  Issue : 2  |  Page : 28-42
Noise and drug induced cochlear damage leads to functional reorganisation in the central auditory system

1 Hearing Research Laboratory, Department of Communicative Disorders & Sciences , University at Buffalo, Buffalo, NY 14214; Department of Neurology, University at Buffalo, Buffalo, NY 14214, USA
2 Hearing Research Laboratory, Department of Communicative Disorders & Sciences , University at Buffalo, Buffalo, NY 14214, USA

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How to cite this article:
Salvi RJ, Wang J, Lockwood AH, Burkard R, Ding D. Noise and drug induced cochlear damage leads to functional reorganisation in the central auditory system. Noise Health 1999;1:28-42

How to cite this URL:
Salvi RJ, Wang J, Lockwood AH, Burkard R, Ding D. Noise and drug induced cochlear damage leads to functional reorganisation in the central auditory system. Noise Health [serial online] 1999 [cited 2019 Sep 20];1:28-42. Available from: http://www.noiseandhealth.org/text.asp?1999/1/2/28/31707

  Introduction Top


Noise induced hearing loss has generally been thought of as an exclusively cochlear pathology because the primary histopathology occurs in the sensory hair cells and spiral ganglion neurons. Single-unit studies of noise-exposed animals have shown that damage to both the inner hair cells (IHCs) and outer hair cells (OHCs) elevates auditory nerve fibres thresholds. In addition, auditory nerve fibre tuning curves become much broader than normal when OHCs are damaged or destroyed. These physiological changes are closely associated with several of the primary symptoms of sensorineural hearing loss, such as the elevation of quiet thresholds, poor frequency selectivity and impaired speech discrimination, particularly in a background of noise (Salvi et al., 1983a; Salvi et al., 1983b; Wightman, 1982). However, several symptoms of noise-induced hearing loss cannot be accounted for based on cochlear electrophysiology. For example, tinnitus, the perception of sound in the absence of an acoustic stimulus, was thought to originate from hyperactivity in the auditory nerve. However, there is little evidence of spontaneous hyperactivity in the auditory nerve after noise­induced cochlear damage (Salvi et al., 1983a; Salvi et al., 1983b). In fact, transection of the auditory nerve often gives rise to tinnitus. This suggests that many cases of tinnitus have a central, rather a cochlear, origin. Another symptom that is difficult to account for based on cochlear pathology is the abnormally rapid growth of loudness, or loudness recruitment (Hallpike and Hood, 1960; Zeng and Turner, 1991). When the sensory hair cells are damaged by acoustic trauma or ototoxic drugs, the maximum neural output of the cochlea is reduced and the slope of the amplitude-level function decreases (Salvi et al., 1979a; Salvi et al., 1979b). This suggests that the neural correlates of loudness recruitment may exist at higher levels of the auditory pathway. In this chapter, we will review the physiological data that suggests that tinnitus, loudness recruitment and hyperacusis may result from functional reorganisation in the central auditory pathway.

Functional Reorganisation:

Although a great deal is known about the physiological changes that occur in the cochlea when the cochlea is damaged (Salvi et al., 1983b; Salvi et al., 1983c), relatively little is known about the functional changes that occur in the central auditory pathway. Results from other sensory systems suggest that damage to the peripheral receptor surface can cause rather profound changes in the functional properties of neurons in the central nervous system. A striking example of this is the rapid reorganisation that occurs in neurons of the somatosensory cortex when receptors in a segment of the body surface are inactivated by anaesthesia or amputation (Calford and Tweedale, 1988). [Figure - 1] shows the excitatory receptive field of a neuron in the somatosensory cortex of the flying fox (bat). Normally, the neuron responds in an excitatory manner when mechanical stimulation is delivered to a digit on the wing (black area). Consequently, when the digit is amputated, the neuron should be inactivated, or silenced, due to the loss of excitatory inputs. However, digit amputation leads to significant reorganisation of the neuron's receptive field such that it begins to respond to mechanical stimulation delivered to the wing adjacent to the original digit. Because these changes occur within a matter of minutes, they presumably result from the unmasking of pre­existing excitatory inputs to this neuron, i.e. disinhibition. Apparently, the full range of excitatory inputs is limited by inhibitory signals that originate from the center of the original receptive field. In this chapter, our working hypothesis is that damage to a segment (analogous to amputation) of the inner ear can cause significant functional reorganisation in the central auditory pathway in a manner similar to that shown in [Figure - 1].

In the following sections, we will review some of the unexpected signs of functional reorganisation seen in the dorsal cochlear nucleus (DCN), inferior colliculus and auditory cortex (AC) after the cochlea is damaged by acoustic overstimulation or ototoxic drugs. Since most of the studies have been described previously, the discussion will focus on the experimental results and their relationship to several symptoms of sensorineural hearing loss such as loudness recruitment, tinnitus and hyperacusis. Most of the physiological results presented below were obtained from chinchillas. More recently, the studies have been extended to humans by using positron emission tomography (PET) to measure the changes in cerebral blood flow (CBF) in subjects with sensorineural hearing loss and tinnitus.


  Results and Discussion Top


Acoustic Trauma Enhances Evoked Potential Amplitude: A convenient method for monitoring the functional changes that occur in the peripheral and central auditory pathway following cochlear damage is to implant chronic recording electrodes at several different levels of the auditory brain. Local field potentials were measured at the round window (compound action potential, CAP) and inferior colliculus (IC) before and after exposing chinchillas for 5 days to a 105 dB SPL pure tone at 2 kHz (Salvi et al., 1990).

Measurements of evoked response thresholds obtained 30 days or more post-exposure showed that the animals had developed a permanent hearing threshold shift of approximately 30-35 dB around 4 kHz [Figure - 2]A. The threshold shift decreased at higher and lower frequencies so that hearing was essentially normal in the 0.5-1 kHz range and at 16 kHz. Evoked potential amplitude-level functions were also measured to determine what effect the threshold shift had on the magnitude of the suprathreshold responses. [Figure - 2]B shows the amplitude-level function in the region of maximum hearing loss, 4 kHz. Because of the threshold is elevated in the 4 kHz region, higher sound levels are required to elicit a response. However, once threshold is exceeded, the amplitude increases rapidly, catches up to and exceeds the normal response at moderate to high intensities. Thus, the maximum response amplitude is equal to or greater than the pre-exposure maximum at high sound levels. Two aspects of the 4 kHz response are notable. First, the input/output function shows recruitment-like behaviour. This rapid growth of response amplitude could be a neural correlate of loudness recruitment seen in the region of hearing loss (Hallpike & Hood, 1960; Zeng & Turner, 1991). Second, the maximum response amplitude is within the normal range whereas the maximum output of the cochlea is almost certain to be greatly reduced. [Figure - 2]C shows the amplitude-level function at 0.5 kHz, a frequency located two octaves below the exposure frequency. Surprisingly, even though the threshold was normal at this frequency, the amplitude-level function increased at an abnormally rapid rate resulting in a response that was 2-4 times larger than normal at high sound levels. These results suggest that the gain of the central auditory system had increased as a result of cochlear damage. Since the enhancement of maximum response amplitude was nearly always observed on the low frequency side of the hearing loss, we hypothesised that it was due to the loss of lateral inhibition originating from the primary region of damage.

Rapid Onset of Amplitude Enhancement: Important insights regarding the mechanisms that give rise to the enhanced evoked potentials in the IC can be obtained by studying the time course over which the amplitude enhancement develops. [Figure - 3] shows the amplitude-level functions to a 1 kHz tone recorded from the round window (CAP) and the IC following a 2 hr exposure at 2.8 kHz at 105 dB SPL. At 24 hours post-exposure, the CAP amplitude-level function [Figure - 3]A shows a significant reduction in amplitude compared to the pre-exposure measures and the slope of the amplitude-level function is reduced. The IC amplitude-level function, on the other hand, is more complex. At low sound levels, the response amplitude from the IC is reduced; however, once the intensity exceeds 50 dB SPL, the amplitude increases rapidly and eventually becomes much larger than the pre-exposure values. Several aspects of these results are significant. First, since the amplitude of the CAP is smaller than normal, the amplitude enhancement seen in the IC cannot be a cochlear phenomenon. Second, since the amplitude enhancement develops rapidly, in some cases as early as 8 hr post-exposure (Salvi et al., 1996), it most likely involves the unmasking (disinhibition) of pre-existing neuronal circuitry rather than axonal sprouting and formation of new neuronal connections (Calford & Tweedale, 1988).

Lateral Inhibition Model of Enhancement: One of the hallmarks of the auditory pathway is its precise tonotopic organisation. [Figure - 4]A is a schematic that shows the basilar membrane vibration pattern to low, medium and high­frequency tone stimuli and the location of the IHCs along the length of the basilar membrane. Each type I auditory nerve fibre contacts a single IHC in a one-to-one manner. Each auditory nerve fibre sends it terminal axons to the anteroventral cochlear nucleus (AVCN), posteroventral cochlear nucleus (PVCN) and dorsal cochlear nucleus (DCN). For simplicity, only the AVCN is shown in [Figure - 4]. High frequency tones produce a basilar membrane vibration pattern with an amplitude peak that preferentially excites hair cells in the base of the cochlea. Low frequency tones, by contrast, produce maximum vibration near the apex of the cochlea. Low frequency tones can also excite hair cells in the base of the cochlea, but only when the stimulus level is extremely high. Since each auditory nerve fibre contacts a single IHC, the response of a fibre that contacts a hair cell in the base of the cochlea has a V-shaped tuning curve with a low-threshold tip located at the high frequencies and a high-threshold, broadly-tuned, low-frequency tail [Figure - 4]B. The frequency with the lowest threshold on the tuning curve is referred to as the characteristic frequency (CF). A fibre that contacts a hair cell in the apex of the cochlea will have a narrowly tuned tip with a low CF and little or no low-frequency tail. Auditory nerve fibres increase their discharge rate when a tone burst is presented at surprathreshold levels. Significantly, the spontaneous activity of auditory nerve fibres cannot be suppressed by simple pure tone, i.e., there is little evidence of single-tone suppression in mammals.

When an auditory nerve fibre enters the cochlear nucleus, it makes excitatory (E) synaptic contact with many neurons in the same layer of the cochlear nucleus thereby forming a sheet of neurons all tuned to the same frequency or iso­frequency sheet. High frequency iso-frequency sheets are located in dorsally and low-frequency iso-frequency sheets are located ventrally (Rose et al., 1960). Thus, the tonotopic organisation of the cochlea is preserved at higher levels of the auditory brain. Neurons in each iso-frequency sheet can interact with one another in an inhibitory (I) manner. This results in complex response areas that consist of an excitatory tuning curve with a narrowly-tuned V-shaped tip that is surrounded by inhibitory response areas above and below CF [Figure - 4]B (Evans and Nelson, 1973; Young, 1984). In some cases, the inhibitory response can completely envelop the excitatory response area at high sound levels.

The lateral inhibitory areas provide a mechanisms to account for the evoked response amplitude enhancement seen when a segment of the cochlea is damaged by acoustic overstimulation. [Figure - 5]A is a schematic showing the inhibitory and excitatory inputs to a hypothetical auditory neuron in the cochlear nucleus or higher auditory center (Salvi et al., 1998). The inhibitory tuning curve has a CF that is located at a slightly higher frequency than the excitatory tuning curve, but the CF-thresholds for excitation and inhibition are similar. We assume that the central neuron will respond in an excitatory manner when the threshold for the excitatory input is lower than the threshold for the inhibitory input. Conversely, if the threshold for the inhibitory input is lower than that for excitation, then the spontaneous activity of the neuron will be inhibited. [Figure - 5]B shows the excitatory response area of such a model. Note that the excitatory tuning curve is extremely narrow and lacks a low-frequency response area. [Figure - 5]C shows the hypothetical discharge rate­level function of the model at the excitatory CF. At low sound levels, the neuron's discharge rate increases with level. However, once the stimulus level exceeds the threshold in the tail of the inhibitory tuning curve input [Figure - 5]A, the discharge rate begins to decline. As a result, the neuron's discharge rate-level function is non­monotonic resulting in a decrease in discharge rate at high stimulus levels.

[Figure - 6] shows how the output of the model will change when a traumatising tone is presented at a stimulus frequency near the inhibitory CF, but slightly above the excitatory response area. In this case, the traumatising tone will damage a narrow region of the cochlea and selectively increase the threshold of the inhibitory input without affecting the excitatory input. Because the damage is confined to frequencies above the excitatory input, the output of the model will remain largely unchanged near the tip of the output tuning-curve [Figure - 6]B. However, the elevation of the inhibitory input will result in the expansion of the low-frequency tail of the output-tuning curve.

Thus, the low-frequency tail of the tuning curve will be unmasked due to the loss of inhibition. The elevation of the inhibitory threshold will also alter the shape of the discharge rate-level function at CF. The model predicts that the maximum discharge rate and the dynamic range will increase significantly after the exposure.

Acoustic Trauma Alters Response Areas and Discharge Rates Level Functions.

Dorsal Cochlear Nucleus. Since the axons of many neurons in the DCN project to the contralateral IC (Adams, 1979; Osen, 1972), the DCN could conceivably play a major role in regulating the evoked potential amplitude enhancement observed in the IC. Many neurons in the DCN have inhibitory response areas that surround the excitatory response area. [Figure - 7]A shows the response area map of a neuron in the DCN with an excitatory CF of 4545 Hz, a CF-threshold of 15 dB SPL and a spontaneous rate of approximately 2 spikes/s. The black areas and shaded areas show the frequency­intensity combinations that elicit an excitatory and inhibitory response respectively; the height of the bars is approximately equal to the magnitude of the excitatory or inhibitory response. This particular neuron had an inhibitory response area above and below CF and a very narrow excitatory response area with a relatively high threshold in the low-frequency tail. [Figure - 7]B shows how the response area changes after a 6.57 kHz tone (111 dB SPL, 15 minutes) was presented above CF. Even though the traumatising tone was restricted to the inhibitory area above CF, the inhibitory responses above CF and below CF are both greatly attenuated. This suggests that the inhibitory response area below CF receives inputs mainly from a region of the cochlea that is tuned to a higher frequency. Because the inhibitory inputs have been selectively attenuated by the traumatising tone, the excitatory response area shows a significant expansion and improvement in threshold in the low-frequency tail region. Moreover, the spontaneous discharge rate increased from 2 to 16 spike/s and the threshold decreased from 15 to 12 dB SPL.

The loss of inhibition above CF resulted in a dramatic increase in the discharge rate to stimuli in the low frequency tail of the response area. [Figure - 8]A shows the rate-level function to a 556 Hz tone measured before and after the traumatising stimulus. Before the exposure, the neuron failed to respond to the 556 Hz tone except when the level exceeded 75 dB SPL. However, after the exposure, the intensity needed to elicit an excitatory response decreased to approximately 55 dB SPL and the maximum discharge rate increased by roughly a factor of 4.

Collectively, these results are consistent with the model described above and illustrate how the loss of inhibition above CF can affect the response to suprathreshold stimuli, particularly in the tail of the tuning curve. The physiological changes shown in [Figure - 7],[Figure - 8] were most often seen in neurons with inhibitory response areas surrounding the excitatory response area. By contrast, many neurons in the DCN with broad low-frequency tails and that lacked inhibitory response areas above CF were unaffected when the traumatising tones was presented above the excitatory CF.

Inferior Colliculus. A more direct test of the model has been made by examining the tuning curves and discharge rate-level functions of neurons in the IC before and after presenting a traumatising tone above the unit's excitatory CF. [Figure - 9]A shows the tuning curve of a unit that could only be excited by a narrow range of frequencies near it CF, approximately 8 kHz. Since the neuron lacked spontaneous activity, its inhibitory response area could not be evaluated; however, because the excitatory tuning curve was very narrow, we assumed that this neuron was receiving inhibitory inputs from frequencies above its CF. To test this hypothesis, we exposed the ear for 20 minutes to a 107-dB SPL tone at 16.1 kHz. Although the neuron did not respond to the traumatising stimulus, the low-frequency tail of its excitatory tuning curve was substantially altered after the exposure. Low­frequency stimuli that failed to activate the neuron before the exposure now produced a robust response and thresholds along the low­frequency tail of the tuning curve improved by as much as 25 dB. Although there were significant changes in the tail of the tuning curve, the narrow tip and high-frequency side of the tuning curve were unchanged. The discharge rate-level functions near CF also showed an increase in the maximum driven rate after the traumatising exposure [Figure - 9]B. These changes are consistent with the model described above. Approximately 40% of the neurons in the IC showed an expansion of their tuning curves and an increase in the maximum driven rate following the exposure. These neurons generally had very narrowly tuned excitatory response areas and non-monotonic discharge rate-level functions. Other neurons with monotonic rate-level functions and tuning curves with extended low-frequency tails generally showed little change in their behaviour after the traumatising exposure.

Evidence for Automatic Gain Control in Central Auditory

Pathway. While the lateral inhibition model may accounts for some of the hyperactivity seen in the central auditory pathway following cochlear trauma, recent experimental evidence suggests that other factors may be involved in modulating the gain of the central auditory system when the input from the cochlea is reduced. Evidence favouring some additional gain control mechanisms have been derived from chinchillas with selective IHC lesions produced by the ototoxic drug, carboplatin (Burkard et al., 1997; Trautwein et al., 1996; Wang et al., 1997). Using this preparation, it is possible to selectively destroy some of the IHCs while retaining an intact population of the OHCs. [Figure - 10] shows the percentage of missing IHCs and OHCs from a carboplatin-treated chinchilla. In contrast to other ototoxic drugs, carboplatin tends to selectively destroy IHCs along the length of the cochlea while sparing the OHCs in the chinchilla. To confirm that the surviving OHCs are functionally intact in these carboplatin­treated chinchillas, the cochlear microphonic potential and the distortion product otoacoustic emissions were measured. The cochlear microphonic potential and distortion product emissions were completely normal in ears with massive IHC loss, but intact OHCs (Trautwein et al., 1996). It has been possible to record from auditory nerve fibres that contact the surviving IHCs to assess their functional integrity. Remarkably, the surviving auditory nerve fibre­IHC complex retains its normal sensitivity and tuning with IHC lesions as large as 60-70% (Wang et al., 1997). Since the IHCs provide the only pathway for transmitting information from the cochlea to the central auditory system, an ear with a 50% selective IHC loss should transmit roughly 50% less information to the central auditory pathway. Measurements of the CAP confirm that the amplitude is reduced in proportion to the amount of IHC loss (Wang et al., 1997).

The IHC-lesion model provides a unique opportunity to determine how the central auditory system responds to a unique form of sensory deprivation in which there are a reduced number of auditory nerve inputs, each of which has retained its normal threshold and tuning. To address this issue, the local field potentials in the IC and AC were measured before and after selectively destroying a portion of the IHC population. The top panel in [Figure - 11] shows the IC input/output functions before and 3 days, 2 weeks and 5 weeks after carboplatin treatment. For ease of comparison, amplitudes are expressed as a percentage of the maximum pre-exposure values. The post-carboplatin amplitudes are reduced at high intensities at all three recording times, consistent with the hair cell lesion. However, at low intensities (<45 dB SPL), the amplitudes are remarkably normal despite the large IHC lesion. The bottom panel of [Figure - 11] shows the pre- and post-carboplatin input/output functions from the AC of the same animal. The time course of the amplitude change is complex. At 3 days post-carboplatin, the amplitudes are completely normal. Surprisingly, at 2 weeks post-carboplatin, the AC amplitudes are much larger than normal despite the IHC lesion and reduced input from the IC. Finally, at 5 weeks post-carboplatin, the AC amplitudes were still slightly larger than normal. Several features of the data are significant. First, the ability of the AC to produce a larger than normal response when the input from the cochlea is reduced is remarkable and suggests that some form of gain control mechanism must be operating to compensate for the reduced input. Second, the change in AC amplitude varies over time, first overshooting and then falling back towards the normal range. This suggests that the gain control mechanism attempts to keep the response of the auditory cortex operating in its optimal physiological range despite the change in peripheral inputs. Control mechanisms similar to these have been observed in other systems (Davis and Goodman, 1998; Turrigiano et al., 1998).

Evidence of Hyperactivity in the Human Auditory Cortex.

With the rapid advances made in brain imaging techniques over the past few decades, it has become possible to assess the functional activity in the human auditory cortex. Based on the electrophysiological data obtained in the chinchilla, we hypothesised that the activation of the AC of humans with cochlear hearing loss would be greater than that observed in normal subjects. To test this hypothesis, we used positron emission tomography (PET) and 15O labelled water to measure the change in local cerebral blood flow (CBF) in normal­hearing subjects and subjects with high­frequency sensorineural hearing loss and tinnitus (Lockwood et al., 1998). The data were evaluated using Statistical Parameter Mapping (SPM 95) techniques. Since the brain has no energy reserves, any local increase in neural activity (e.g., listening to a sound) will cause an increased metabolic demand that results in an increase in local CBF, i.e., activation.

On the basis of our electrophysiological measurements, we predicted that a 2 kHz-tone burst (right ear, insert earphone, 80 dB SPL, 500 ms on, 500 ms off, 2 minute presentations) would activate more of the brain in our patients than in our control subjects with normal hearing. The patients (n=4) had a 40-70 dB hearing loss in the 4-8 kHz region. Patients and normal control subjects had similar hearing thresholds at 2 kHz and below. [Figure - 12]A shows the regions in the left hemisphere of the brain where there was a significant increase in blood flow, relative to the resting state. Sites of significant activation have been projected on to the lateral surface of a MRI image of a human brain. A similar pattern of activation was seen in the left hemisphere. The active regions included the right and left superior temporal gyri (Brodmann area 22, BA 22) and the right and left transverse temporal gyri (BA 41. To determine whether the 2 kHz tones activated more of the brain in the patients than in the controls, we subtracted the activation found in the controls from the activation observed in the patients using the SPM contrast: patient (2 kHz -rest) - control (2 kHz -rest). By controlling for possible differences in the resting state associated with tinnitus, this analysis eliminates the possible confounding effects of these phantom auditory sensations. As shown in [Figure - 12]B, additional areas of activation are present in the auditory cortex of patients compared to controls. These results are consistent with the evoked potential data from animals with noise-induced hearing loss. It is possible, however, that tinnitus, combined with the sensorineural hearing loss led to the plastic changes (i.e., additional activation) seen in these patients.

It has long been known that cochlear damage caused by noise exposure or ototoxic drugs reduces the neural output flowing of the cochlea into the central auditory system (Eldredge et al., 1973; Salvi et al., 1979b). Severe cochlear damage reduces the number of spontaneously active neurons and the number of neurons that respond to sound thereby reducing the flow of information into the central auditory system. It has generally been assumed that a reduced neural output from the cochlea would translate into a reduced neural response in the central auditory system. However, the results presented above show that is not always the case. Ears with significant cochlear damage often show a rapid increase in neural activity in the central auditory pathway once threshold is exceeded. Consequently, the response from the central auditory pathway is sometimes equal to or even greater than in the normal ear. The rapid growth of physiological responses observed in the central auditory pathway mirror the rapid growth of loudness seen in some patients with sensorineural hearing loss. In addition, the physiological responses in the central auditory pathway are sometimes much larger than normal. These abnormally large responses could conceivably contribute to hyperacusis and loudness tolerance problems observed in some patients with cochlear hearing loss. Finally, some neurons in the central auditory pathway show an increase in their spontaneous discharge rates. Thus, the hyperactivity observed in the central auditory system may also play a role in generating the phantom auditory perception known as tinnitus.

Acknowledgements:

Work supported in part by a grant from NIH (1 R01 DC03306-01A1).[24]

 
  References Top

1.Adams JC (1979) Ascending projections to the inferior colliculus. Journal of Comparative Neurology. 182, 519­-538.  Back to cited text no. 1    
2.Burkard R, Trautwein P and Salvi RJ (1997) The effects of click level, click rate, and the level of background masking noise on the inferior colliculus potential (ICP) in the normal and carboplatin-treated chinchilla. J. Acoust. Soc. Am. 102, 3620-3627.  Back to cited text no. 2    
3.Calford MB and Tweedale R (1988) Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature. 332, 446-­448.  Back to cited text no. 3    
4.Davis GW and Goodman CS (1998) Synapse-specific control of synaptic efficacy at the terminals of a single neuron. Nature. 392, 82-86.  Back to cited text no. 4    
5.Eldredge DH, Mills JH and Bohne BA (1973) Anatomical, behavioral, and electrophysiological observations on chinchillas after long exposures to noise. Advances in Oto-Rhino-Laryngology. 20, 64-81.  Back to cited text no. 5    
6.Evans EF and Nelson PG (1973) The response of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state. Experimental Brain Research. 17, 402-427.  Back to cited text no. 6    
7.Hallpike CS and Hood JD (1960) Observations on the neurological mechanism of the loudness recruitment phenomenon. Acta Otolaryngologica (Stockholm). 50, 472-486.  Back to cited text no. 7    
8.Lockwood AH, Salvi RJ, Coad ML, Towsley MA, Wack DS and Murphy BW (1998) The functional neuroanatomy of tinnitus: Evidence for limbic system links and neural plasticity. Neurology. 50, 114-120.  Back to cited text no. 8    
9.Osen KK (1972) Projection of the cochlear nuclei on the inferior colliculus in the cat. Journal of Comparative Neurology. 144, 355-372.  Back to cited text no. 9    
10.Rose JE, Galambos R and Hughes J Organisation of frequency sensitive neurons in the cochlear nucleus complex of the cat in GL Rasmussen and WE Windle (eds.) (1960) Neural Mechanisms of the Auditory and Vestibular System. Springfield: Thomas pp. 116-136.  Back to cited text no. 10    
11.Salvi R, Hamernik RP and Henderson D (1979a) Auditory nerve fibre activity and cochlear morphology after noise trauma. Acta Otolaryngology. 224, 111-116.  Back to cited text no. 11    
12.Salvi R, Henderson D and Hamernik RP (1979b) Single auditory nerve fibre and action potential latencies in normal and noise-treated chinchilla. Hearing Research. 1, 237-251.  Back to cited text no. 12    
13.Salvi RJ, Henderson D, Hamernik R and Ahroon WA (1983a) Neural correlates of sensorineural hearing loss. [Review] [40 refs]. Ear & Hearing. 4, 115-129.  Back to cited text no. 13    
14.Salvi RJ, Henderson D and Hamernik RP Physiological basis of sensorineural hearing loss in J Tobias and E Schubert (eds.) (1983b) Hearing Research and Theory. New York: Academic Press pp. 173-231.  Back to cited text no. 14    
15.Salvi RJ, Henderson D, Hamernik RP and Ahroon WA (1983c) Neural correlates of sensorineural hearing loss. Ear and Hearing. 4, 115-129.  Back to cited text no. 15    
16.Salvi RJ, Saunders SS, Gratton MA, Arehole S and Powers N (1990) Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma. Hearing Research. 50, 245-258.  Back to cited text no. 16    
17.Salvi RJ, Wang J and Powers N Rapid functional reorganisation in the inferior colliculus and cochlear nucleus after acute cochlear damage in RJ Salvi, D Henderson, F Fiorino and V Colletti (eds.) (1996) Auditory Plasticity and Regeneration. New York: Thieme Medical Publishers pp. 275-296.  Back to cited text no. 17    
18.Salvi RJ, Wang J and Qiu C-X Evidence for functional reorganisation in the central auditory system after acoustic overstimulation in L Luxon and D Prasher (eds.) (1998) Advances in Noise Research Volume I: Biological Effects of Noise.: Whurr Publishers LTD pp. 29-42.  Back to cited text no. 18    
19.Trautwein P, Hofstetter P, Wang J, Salvi R and Nostrant A (1996) Selective inner hair cell loss does not alter distortion product otoacoustic emissions. Hearing Research. 96, 71-82.  Back to cited text no. 19    
20.Turrigiano GG, Leslie KR, Desai NS, Rutherford LC and Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 391, 892-896.  Back to cited text no. 20    
21.Wang J, Powers NL, Hofstetter P, Trautwein P, Ding D and Salvi RJ (1997) Effect of selective IHC loss on auditory nerve fibre threshold, tuning, spontaneous and driven discharge rate. Hearing Research. 107, 67-82.  Back to cited text no. 21    
22.Wightman FL Psychoacoustic correlates of hearing loss in RP Hamernik, D Henderson and RJ Salvi (eds.) (1982) New Perspectives on Noise-Induced Hearing Loss. New York: Raven Press pp. 375-394.  Back to cited text no. 22    
23.Young E Response characteristics of neurons of the cochlear nucleus in C Berlin (ed.) (1984) Hearing Science. San Diego: College-Hill pp. 423-460.  Back to cited text no. 23    
24.Zeng FG and Turner CW (1991) Binaural loudness matches in unilaterally impaired listeners. The Bimonthly Journal of Experimental Psychology. 43A, 565-583.  Back to cited text no. 24    

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Correspondence Address:
Richard J Salvi
Hearing Research Laboratory, Department of Communicative Disorders & Sciences , University at Buffalo, Buffalo, NY 14214; Department of Neurology, University at Buffalo, Buffalo, NY 14214
USA
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Source of Support: None, Conflict of Interest: None


PMID: 12689506

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