Perceptual Consequences of Disrupted Auditory Nerve Activity FAN-GANG ZENG, YING-YEE KONG, HENRY J MICHALEWSKI, AND ARNOLD STARR Journal of Neurophysiology.

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Perceptual Consequences of Disrupted Auditory Nerve Activity FAN-GANG ZENG, YING-YEE KONG, HENRY J MICHALEWSKI, AND ARNOLD STARR Journal of Neurophysiology Vol:93;2005 Presenters: Anusha Ramesh & Bijan Saikia Guides: Mr. Animesh Barman & Mr. Ajith Kumar.

Introduction Perception is a delicate chain of events that includes conversion of a sensory stimulus into electrical signals and processing and interpretation of the electrical signal in the CNS. Electric stimulation of the auditory nerve via a cochlear implant in persons with hearing impairment results in fundamental changes in the brain affecting behaviors ranging from basic psychophysics to language development. Clinically, these studies often lead to better diagnosis and management of a particular disease. Theoretically, these studies shed light on the relative contribution of different neural codes to perception at a mechanism level.

The clinical diagnosis of AN has been typically characterized by the presence of otoacoustic emission and/or cochlear microphonics and the concurrent absence of the averaged auditory brainstem responses. Despite absent auditory brainstem responses, it is evident that sound information must have been transmitted because individuals with AN can hear sound, have normal brain imaging, and identifiable although usually delayed cortical potentials (Rance et al. 2002; Starr et al. 2003; Zeng et al. 1999).

The distorted auditory nerve activity has been suggested in the form of :  desynchronized or  reduced discharge in the auditory nerve.  Desynchronized neural discharge can occur due to demyelination and ion-channel dysfunction in the auditory nerve and/or dysfunctional synaptic transmission between the inner hair cells and the auditory nerve. Loss of the neural input to the brain can occur due to inner hair cell loss and/or auditory nerve loss.

Although the term AN has been widely accepted clinically as a diagnosis, alternative terms such as "auditory dys-synchrony" have been suggested to reflect the common phenomenon The prevalence of AN has been estimated to be as high as 10% of the children identified as having hearing loss (Berlin et al. 2003a; Rance et al. 1999). Because AN patients typically do not derive benefits from conventional hearing aids, treatment options are limited with only recent success being reported with cochlear implantation.

 Limited behavioral data have been reported on the perceptual consequences of auditory neuropathy.  Kraus et al. noted in their case study that the AN subject had a nearly normal audiogram but significant difficulty in speech perception in noise.  Zeng et al. (1999) found significant temporal processing impairment in 8 AN subjects and were able to correlate the degrees of their temporal processing impairment with the degrees of their speech perception deficits.  Rance et al. (2004) found additional frequency discrimination deficits in some of their 14 AN subjects, who also had concurrent temporal processing impairment.

Aim To examine perceptual consequences of disrupted auditory nerve activity in subjects with auditory neuropathy. To report psychophysical data in basic auditory processing in: Intensity Frequency Time

Method Subjects:  21 AN subjects(13 females, 8 males)  Age range: 6 to 53yrs(mean=21yrs)  Hearing threshold:20dBHL to 70dBHL

OAE: 16/19 subjects Cochlear microphonics: 19/20 subjects Absent/abnormal ABR: all 21 subjects Absent middle ear reflex: 17 tested subjects Distorted/delayed cortical potentials: 15/17 subjects

Brain imaging: normal CNS: 13/21 subjects Neurological examination: peripheral neuropathy:7/21 subjects Control group: 34 age matched normal hearing subjects

STIMULI: All stimuli were generated digitally using TDT system II equipments (Tucker-Davis Technologies,Gainesville) A 16 bit D/A converter was used with a 44,100 Hz sampling rate. A 2.5ms ramp was applied to all stimuli. The full digital range was used to generate a 1000 Hz calibration tone that reached a maximum level of 100dBSPL.

The subjects performed all tasks in a double walled, sound attenuating booth Three sets of experiments were conducted to characterize fundamental detection and discrimination abilities in AN subjects Intensity JND: threshold to MCL- 200ms, 1000Hz tone.

Frequency JND: MCL-200ms, 250 to 8000Hz tone. Temporal processing: Temporal integration(5 to 500ms) Gap detection(5 to 50dBSL) Temporal modulation(2 to 2000Hz at MCL)

Psychophysical procedure: An adaptive, three- interval, three-alternative, forced-choice, two-down and one-up procedure was employed to track correct response criterion (Levitt 1971) Subjects heard three sounds that were visually marked by three intervals on a computer screen One of the three intervals contained the signal, whereas the other two contained the standard. The order of the signal and the standard sounds was randomized (3-alternative ).

The subject had to choose the signal (forced- choice) and was given a visual feedback regarding the correct response. The initial difference between the signal and the standard was large so it was easy for the subject to tell which interval contained the signal. The difference was reduced after two consecutive correct responses and increased after one incorrect response (2-down, 1-up).

Statistical analysis: A between –subjects ANOVA with uneven sample sizes with posthoc tests were done.

Results: Intensity discrimination:

Frequency discrimination

Figure shows frequency discrimination as a function of standard frequency in 12 AN subjects and 4 normal controls. A significant difference in performance was observed between the AN subjects and the normal controls The normal controls required less than 10 Hz to discriminate a pitch difference for frequencies at or less than 1,000 Hz but the AN subjects required a difference that was about 2 orders of magnitude higher than the normal difference limen. The difference between the two groups reduced with frequency and was not significant at 8,000 Hz This result suggests that AN subjects have profound impairment in pitch discrimination at low frequencies ( 4,000 Hz).

Temporal processing Figure shows temporal integration as a function of duration in 16 AN subjects and 4 normal controls. Both AN and normal-hearing subjects showed a 100-to-200 ms course of temporal integration, but the slope of the temporal integration function was slightly elevated in the AN subjects as compared with the normal-hearing subjects A between-subjects ANOVA revealed a significant group effect between the AN and normal-hearing subjects but a post-hoc t-test revealed a significant difference only for the 5- and 10-ms sounds. This result indicates that AN subjects have difficulty detecting short sounds but not long sounds.

Figure shows gap detection as a function of sensation level in 20 AN subjects and 7 normal controls There was a significant group effect between the AN and the control subjects The normal controls required about a 50-ms silent interval to detect a gap at 5-dB low sensation (very soft sound) but improved to 3 ms at high sensation levels (40 and 50 dB). The AN subjects performed similarly to the normal controls at low sensation levels (5 and 10 dB) but required significantly longer gaps (15-20 ms) than the normal- hearing subjects at higher sensation levels. This result suggests that the AN subjects have difficulty in gap detection even at comfortable loudness levels.

Figure shows modulation detection as a function of modulation frequency in 16 AN subjects and 4 normal controls. There was a significant difference between the two groups but no significant interactions between groups and modulation frequency. The normal controls showed a typical low-pass pattern, with peak sensitivity of –19.9 dB (10% modulation) and 3-dB cutoff frequency of Hz. The AN subjects showed a lower peak sensitivity of –8.7 dB (37% modulation) and a lower cutoff frequency of 17.0 Hz. The relatively poor fit in AN subjects was due to the band- pass characteristic in the data. This result suggests that AN subjects have difficulty in detecting both slow and fast temporal modulations.

DISCUSSION The perceptual consequences of disrupted auditory nerve activity in 21 subjects with auditory neuropathy have been studied and the result was that the auditory perception related to intensity perception is relatively normal. On the other hand auditory perception related to temporal processing is significantly impaired.

Comparisons with other hearing disorders ParametersCochlear damageAuditory neuropathy Intensity discrimination Changes: - Steeper than normal loudness growth. - better discrimination at equal sensation level No significant changes. -slightly worsens performance at low sensation levels Frequency discrimination Impairs uniformly Impairs selectively Temporal processing Usually not impairedUsually impaired

Physiological mechanisms The term auditory neuropathy was coined because many of the subjects initially studied had some form of peripheral neuropathy based on neurological examinations (Starr et al. 1996). The site of lesion for auditory neuropathy includes all possible combinations of the inner hair cells, the synapse between the inner hair cell n auditory nerve and the auditory nerve itself (Hallpike et al. 1980). The lesion on these sites can lead to two neurophysiologic manifestations including: 1 Desynchronized spikes. 2 Reduced spike count. The desynchronized auditory nerve activity is likely to produce abnormal response in the brainstem neurons that detect coincident firing of auditory nerve fibers. These physiological mechanisms may underlie the observed perceptual changes in auditory neuropathy subjects.

Normal auditory pathway converting the “gap” stimuli via three synchronized nerve fibers into an undistorted central representation of the gap at the output

Auditory neuropathy model with desynchronized nerve conduction,in which the central representation of the gap is distorted due to different delays.

Auditory neuropathy model with reduced nerve conduction in which the central representation of the gap is difficult to detect because of its similarity to the background spontaneous activity.

In most of the cases with auditory neuropathy, both desynchronized and reduced spikes may co-exist to exaggerate the perceptual consequences of neural synchrony. The intensity perception is not critically dependent on phase locking information or optimal combination of information from a large group of nerve fibers. Frequency discrimination, particularly at low frequencies, is critically dependent on the presence of inner hair cells (Nienhys and Clark 1978).

Requires both phase locking and combinatorial information from many nerve fibers(Heinz et al 2001). It is apperent that the desynchronized neural activity impairs temporal processing but, it is less apperent how reduced spike count can also impair temporal processing. At low levels, sound would likely activate a small number of nerve fibers in both normal and neuropathy cases

However as the level is increased, The sound would recruit and activate more nerve fibers in normal hearing subjects but, not in auditory neuropathy subjects. This is due to the reduced number of receptors, nerve fibers, or both. Therefore, the gap detection improves with the level in normal hearing subjects but not in auditory neuropathy subjects. In the desynchronized spike model, the detection threshold can be significantly increased because the more sensitive phase-locking cue is absent; the less sensitive overall rate cue has to be used (Colburn et al 2003).

In the receptor / neuron loss model, the detection threshold can be significantly increased because there is essentially a hole or a dead region in the cochlea, forcing the subject to use a less sensitive ‘off-frequency’ cue (Moore 2004). Many of the auditory neuropathy subjects are expected to receive a cochlear implant. So future studies using electrical stimulation of the auditory nerve might help differentiate the site of lesion in auditory neuropathy. The cochlear implants would be able to effectively stimulate the residual neurons restoring the evoked brainstem potentials.

Critical evaluation This study sheds light into better diagnosis and treatment options for persons with auditory neuropathy. Lot of psychophysical studies have been done for better diagnosis and management of auditory neuropathy. Speech perception has not been focused upon. The model explains only gap detection.

Gap detection at high sensation levels- effective means of screening auditory neuropathy. Conventional hearing aids- less benefit, especially in noisy conditions.

These perceptual data suggest innovative signal processing algorithms for improved performance in auditory neuropathy. To eliminate low frequency but preserve or emphasize high frequency components in speech To accentuate the temporal waveform modulation in speech to compensate for impaired temporal processing. Another treatment option is cochlear implantation.

Summary  Perceptual consequences of auditory neuropathy is significantly different from cochlear damage.  Intensity discrimination: near normal  Frequency discrimination: impaired at low frequencies(<4000Hz) near normal at high frequencies(>4000Hz)

 Temporal processing: low sensation level: near normal high sensation level: impaired  Two auditory neuropathy models based on the results have been proposed.  Thus the results suggest several translational research ideas that can improve the diagnosis and treatment of auditory neuropathy.

Conventional hearing aid modification: eliminate low frequency, emphasize high frequency. accentuate temporal waveform modulation in speech. Electrical stimulation: cochlear implant brainstem implant