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A neuroethological theory of the operation of the inferior colliculus.

A general statement of the function of the inferior colliculus is lacking, even after more than three decades of electrophysiological investigation. A neuroethological theory is proposed that accounts for a large and diverse body of evidence. Although aimed at characterizing the inferior colliculus in mammals, the theory also applies generally to the auditory midbrain in vertebrates. The theory has two hypotheses: (1) Tuning processes in the inferior colliculus are related to the biological importance of sounds. (2) There is a change in timing properties at the inferior colliculus, from rapid input to slowed output; this transformation is related to the timing of specific behaviors. Expressed in neuroethological terms, at least some neurons in the inferior colliculus are tuned to sign-stimuli, and the processing of these sign stimuli triggers fixed action patterns for hunting, escape or vocal communication. The resulting temporal transformation adjusts the pace of sensory input to the pace of behavior. Evidence for the theory comes from anatomical, neurophysiological and behavioral studies and includes: (1) massive convergence of parallel auditory pathways at the inferior colliculus, (2) interaction of the inferior colliculus with motor systems, (3) tuning of auditory midbrain neurons to biologically important sounds, (4) the slow pace of neural processing at the inferior colliculus, (5) the slow pace of motor output. The theory has the following implications. Neurons in the inferior colliculus are filters for sounds that require immediate action, such as certain sounds made by prey, predators or conspecifics. Neural processing in the inferior colliculus is species specific, resulting in filtering for these kinds of sounds. Specific action patterns should be correlated with the activity of neurons in the inferior colliculus. Motor activities may modify neural processing in inferior colliculus neurons. The rate at which information is transmitted to the thalamus is regulated by the inferior colliculus.

Animals↗

Auditory evoked potentials for the assessment of noise induced hearing loss.

As it has been demonstrated in many animal experiments, noise can damage the cochlea and the central auditory pathways. It is very difficult in clinical studies to separate the relative contribution of both these sites. Auditory evoked potentials ABR, MLR and SVR study retrocochlear nervous conduction and collectively the results of these techniques proved an objective evaluation of the cochlear function. The Authors have studied a group of 130 sport shooters with high frequency hearing loss and found that in 38 ears a clear retrocochlear component could be recognised. Correlation with intensity, frequency and length of exposure to the traumatic noise demonstrates that explosive noise is an agent for NIHL. However athletes exposed to similar noises did not suffer from similar hearing loss, probably because of the well known individual noise susceptibility.

Adult↗

Efferent desensitization of auditory nerve fibre responses in the cochlea of the turtle Pseudemys scripta elegans.

Extracellular recordings were made from single auditory afferents in the isolated half-head of the turtle, and changes in their acoustic sensitivity were examined following electrical stimulation of the efferent fibres to the basilar papilla. Short trains of efferent shocks caused a prolonged elevation of the pure tone thresholds of the auditory afferents and an abolition of their spontaneous activity. These changes could be demonstrated in a majority of recordings and without antidromic firing of the afferent. The amount of desensitization increased steeply with shock number and a train of ten closely spaced shocks could elevate the threshold at the most sensitive or characteristic frequency by four orders of magnitude. Desensitization also occurred with single efferent shocks at repetition frequencies exceeding 25/s. Discharge rate versus sound pressure functions were constructed for a number of afferents. The maximum slope of the functions, and the saturated firing rates were both reduced by efferent stimulation; there was also an over-all shift of the rate-intensity function to higher stimulus levels. Such effects would enable the afferent to signal a wider range of sound pressures. Efferent stimulation caused a broadening of the afferent frequency-threshold curves by removal of the narrowly-tuned region around the characteristic frequency. We suggest that the loss in tuning and concomitant improvement in temporal resolution may be a functionally important consequence of efferent action.

Acoustic Stimulation↗

Phencyclidine (PCP): effects on auditory evoked potentials in the rhesus monkey.

Effects of acute and chronic administration of phencyclidine (PCP) on auditory evoked potentials (AEPs) were studied in rhesus monkeys with encephalic electrodes permanently implanted. AEPs were evoked by single clicks (1.0 pps in frequency) generated by an externally triggered audiomonitor. Single PCP injections (dose, 2.0 or 4.0 mg/kg IV) in monkeys produced a striking distortion in the amplitudes of major AEP components. This AEP distortion was manifested in superior temporal cortex (ST) by a complex pattern of amplitude reduction and enhancement, and was manifested in the medial geniculate body (MGB) by amplitude reduction. These effects persisted for 4 to 5 hours. Upon chronic administration (dose, 4.0 mg/kg IV daily), the effects of PCP on AEP components in ST were enhanced while little change was noted in its effect on AEP components in MGB. These results suggest that PCP administration in rhesus monkeys causes a significant disturbance of AEPs within central nervous system structures associated with auditory processing (i.e., ST and MGB), and that chronic PCP administration enhances its effects on AEPs predominantly in the primary auditory cortex while having little additional effects on AEPs from the subcortical auditory pathways.

Animals↗

Hearing loss and cochlear abnormalities in the congenital hypothyroid (hyt/hyt) mouse.

The congenital hypothyroid (hyt/hyt) mouse has been described as having a homozygous recessive mutation of a single locus on chromosome 12 which results in significant endocrine hypofunction and retarded growth. Although a distinct correlation between inherited hypothyroidism and hearing loss in humans exists, there has been no previous evaluation of the auditory system in these mutant mice. We determined hearing thresholds by auditory-evoked brainstem response testing and noted a 40-45 dB elevation in the hyt/hyt mouse compared to littermate heterozygote (hyt/+) animals and normal progenitor controls BALB/cByJ (+/+). Conventional light microscopy was used to examine the general anatomy of the cochlea in these animals, and the surface structure of the organ of Corti was further evaluated with scanning electron microscopy. Heterozygote and normal control mice had no significant abnormalities of the cochlea, however the hyt/hyt mice displayed consistent morphologic abnormalities of the stereocilia on both inner and outer hair cell systems. The surrounding and supporting cells were identified in the cochleas of the hypothyroid mouse and control animals and showed no significant histologic abnormalities. The auditory, histologic, and ultrastructural characterization of this model provides a foundation for evaluating the effects of true inherited hypothyroidism on auditory pathway development.

Animals↗

The perception of coherent and non-coherent auditory objects: a signature in gamma frequency band.

The pertinence of gamma band activity in magnetoencephalographic and electroencephalographic recordings for the performance of a gestalt recognition process is a question at issue. We investigated the functional relevance of gamma band activity for the perception of auditory objects. An auditory experiment was performed as an analog to the Kanizsa experiment in the visual modality, comprising four different coherent and non-coherent stimuli. For the first time functional differences of evoked gamma band activity due to the perception of these stimuli were demonstrated by various methods (localization of sources, wavelet analysis and independent component analysis, ICA). Responses to coherent stimuli were found to have more features in common compared to non-coherent stimuli (e.g. closer located sources and smaller number of ICA components). The results point to the existence of a pitch processor in the auditory pathway.

Acoustic Stimulation↗

The use of intravenous lignocaine in the diagnosis and treatment of tinnitus.

The effect of intravenous lignocaine upon the symptom of tinnitus has been assessed in seventy-eight patients and the results correlated with associated hearing loss. Lignocaine appears to be highly effective in suppressing tinnitus in patients with presumed damage or degeneration of the Organ of Corti and is less effective in other groups. It is postulated that tinnitus in patients with Organ of Corti damage is the result of abnormal hyperactivity in the auditory pathway following deafferentation.

Auditory Threshold↗

Deafness-related plasticity in the inferior colliculus: gene expression profiling following removal of peripheral activity.

The inferior colliculus (IC) is a major center of integration in the ascending as well as descending auditory pathways, where both excitatory and inhibitory amino acid neurotransmitters play a key role. When normal input to the auditory system is decreased, the balance between excitation and inhibition in the IC is disturbed. We examined global changes in gene expression in the rat IC 3 and 21 days following bilateral deafening, using Affymetrix GeneChip arrays and focused our analysis on changes in expression of neurotransmission-related genes. Over 1400 probe sets in the Affymetrix Rat Genome U34A Array were identified as genes that were differentially expressed. These genes encoded proteins previously reported to change as a consequence of deafness, such as calbindin, as well as proteins not previously reported to be modulated by deafness, such as clathrin. A subset of 19 differentially expressed genes was further examined using quantitative RT-PCR at 3, 21 and 90 days following deafness. These included several GABA, glycine, glutamate receptor and neuropeptide-related genes. Expression of genes for GABA-A receptor subunits beta2, beta3, and gamma2, plus ionotropic glutamate receptor subunits AMPA 2, AMPA 3, and kainate 2, increased at all three times. Expression of glycine receptor alpha1 initially declined and then later increased, while alpha2 increased sharply at 21 days. Glycine receptor alpha3 increased between 3 and 21 days, but decreased at 90 days. Of the neuropeptide-related genes tested with qRT-PCR, tyrosine hydroxylase decreased approximately 50% at all times tested. Serotonin receptor 2C increased at 3, 21, and 90 days. The 5B serotonin receptor decreased at 3 and 21 days and returned to normal by 90 days. Of the genes tested with qRT-PCR, only glycine receptor alpha2 and serotonin receptor 5B returned to normal levels of expression at 90 days. Changes in GABA receptor beta3, GABA receptor gamma2, glutamate receptor 2/3, enkephalin, and tyrosine hydroxylase were further confirmed using immunocytochemistry.

Animals↗

Effects of prenatal alcohol exposure and aging on auditory function in the rat: preliminary results.

This study investigated select aspects of peripheral and central auditory dysfunction, as well as the pathological effects of aging, In an animal model of fetal alcohol syndrome (FAS). Pregnant rats consumed liquid alcohol diets containing 0, 17.5, or 35% ethanol-derived calories, from gestation day 7 to parturition. A fourth group was untreated. Offspring of these mothers were tested for auditory and neurological function, using the auditory brainstem response at 6, 12, and 18 months of age. Some animals in the alcohol-exposed groups showed a peripheral auditory disorder in the form of congenital sensorineural hearing loss. This was correlated with punctate lesions and malformed stereocilia on the auditory sensory receptor cells of the inner ear. Alcohol-exposed animals also showed a central auditory processing disorder characterized by prolonged transmission of neural potentials along the brainstem portion of the auditory pathway. Animals in the highest dose group also showed an augmentation in the age-related deterioration of auditory acuity. Thus, increased peripheral and central auditory dysfunctions and pathological deterioration of auditory function in old age may be sequelae of FAS. Such morbidities have important implications for the long-term clinical assessment and management of FAS patients.

Age Factors↗

The acute effects of tetrahydrocannabinol on auditory threshold and frequency resolution in human subjects.

AIMS: The study was designed to investigate the acute effects of ingested tetrahydrocannabinol (THC) on auditory function. METHODS: Eight male subjects (aged 22-30 years), who had previous experience of cannabis use, took part in this study. They performed air conduction pure tone audiometry in both ears over 0.5-8 kHz. A simple test of frequency selectivity by detecting a 4-kHz tone under two masking noise conditions was also carried out in one ear. Three test sessions at weekly intervals were carried out, at the start of which they ingested a capsule containing either placebo, or 7.5 or 15 mg of THC. These were administered in a randomized cross-over, double-blind manner. Auditory testing as described above was carried out 2 hours after ingestion. Blood samples were also obtained at this time point and assayed for delta 9- and 11-OH-THC levels. RESULTS: No significant changes in threshold or frequency resolution were seen with the dosages employed in this study. CONCLUSIONS: This suggests that THC at the plasma levels attained in this study does not have profound effect on the processing of elementary stimuli by the auditory pathway.

Administration, Oral↗

Auditory evoked potentials recorded from the cochlear nucleus and its vicinity in man.

Intracranial responses from the auditory nerve and the cochlear nucleus were recorded from patients undergoing neurosurgical operations during which these structures were exposed. Responses to stimulation of the ipsilateral ear with short tonebursts from the vicinity of the cochlear nucleus show a large surface-negative peak, the latency of which is close to that of peak III in the auditory brain-stem evoked potentials recorded from scalp electrodes. There was also a response to contralateral stimulation, smaller in amplitude and with a longer latency. It is concluded that the cochlear nucleus is the main generator of peak III responses, and that structures of the ascending auditory pathway that are more central than the cochlear nucleus are unlikely to contribute to wave III of the auditory brain-stem evoked potentials.

Brain Stem↗

[Deafness and tinnitus in flare-ups in 10 cases of multiple sclerosis].

Deafness in multiple sclerosis is rare, being reported in less than 1 p. 100 of the cases. Ten cases of deafness associated with tinnitus during acute episodes of multiple sclerosis are presented, the diagnosis being definite in 9 patients and probable, according to McAlpine's criteria, in the tenth case. These were not cases where routine examinations demonstrated a latent hearing defect, but were all patients with sudden, often unilateral, incapacitating deafness during an acute episode of the disease, with regression usually after less than 3 months. Deafness recurred in 3 patients and was the initial symptom in 5 cases. Serial audiometric examinations were performed in most cases together with recordings of various evoked potentials, including early auditory evoked potentials during or after the onset of deafness in all 10 patients. BAEPs abnormalities were noted in 8 and appeared to be correlated more with brain stem demyelinization, as it has been established for a few years, than with the deafness itself. Severe anomalies of auditory evoked potentials regressed after the acute episode in only 1 patient. Lesions of the auditory pathways within the brain stem appear to be the cause of the deafness, as shown by results of auditory tests, which pointed to a central origin. The onset of deafness did not indicate a particular progression of multiple sclerosis.

Adult↗

Auditory neglect and the ear extinction effect in dichotic listening: a reply to Beaton and McCarthy (1993).

In our reply to Beaton and McCarthy (1993), we argue that the issue of ear extinction in dichotic listening also should take into account lesion site and lesion extension. When the lesion is primarily affecting the auditory pathways, the resulting dichotic dysfunction may be an ear extinction effect. However, when the lesion is outside of the auditory system, the absence of reports from one ear may be part of a larger cognitive deficit, involving more complex processes, like orientation and attention. Thus, by constraining the definition of an "ear extinction effect" to a perceptual deficit, Beaton and McCarthy confounds the issue of ear extinction with auditory neglect. In our reply we also present some new data from a patient with a left-sided thalamic pulvinar lesion, contrasting his dichotic listening performance with the patient reported in our original 1991 study.

Adult↗

[Visualization of central auditory processes with functional magnetic resonance tomography].

BACKGROUND: Central auditory processes can be visualized using functional MRI in a non-invasive manner and at high spatial resolution. Acoustic stimulation leads to an increase of blood flow of activated areas in the plane of the superior temporal gyrus. Radiologically, this may be visualized based on the long T2-relaxation time of oxyhemoglobin. PATIENTS: Ten normal-hearing subjects with ages between 28 and 38 years took part in the investigations. They received binaural, monaural right, and monaural left stimulation with pulsed sine tones of 1000 Hz at a pulse rate of 6 Hz and a sound pressure level of 100 dB SPL. Tonotopic organization of the auditory cortex was visualized using stimulation by pulsed sine tones of 500 Hz and 4000 Hz. RESULTS: Following monaural acoustic stimulation, increased activity of the contralateral auditory cortex could be demonstrated in 9 subjects. In one subject, bilateral activity was noted. Concerning the tonotopic organization of the auditory cortex, we could show that the higher frequencies were localized more medially and anteriorly; the lower frequencies were localized more laterally and posteriorly in the superior temporal gyrus. However, considerable overlap was noted. CONCLUSIONS: The overlap of the different frequencies could explain the controversial discussion of the tonotopic organization of the auditory cortex. The results of the monaural acoustic stimulation show clearly the predominant signal increase of contralateral areas in the primary auditory cortex. These results confirm the opinion of the current textbooks that the fiber of the auditory pathways mostly cross. Further investigations using functional MRI are necessary for better understanding of physiological and pathophysiological central-auditory processes.

Acoustic Stimulation↗

Auditory brainstem responses of children with developmental language disorders.

Brainstem auditory evoked potentials (BAEPs) were recorded from 48 children with language disorders (aged four to nine years old, IQs normal to borderline, normal audiometric thresholds and attending special school) and 20 healthy children (four to eight years old, with normal IQs, audiometry and school-level). The language-disabled group showed significantly lower absolute latency values of the BAEPs than controls. There were no significant differences in the central conduction time of the auditory pathway (I-V interval). Therefore, the only significant difference corresponded to a minor value for the first wave (auditory nerve discharge) of the BAEP. A reduction in the control mechanisms of the sensory inputs at the peripheral level, or a disturbance in the inhibitory mechanisms of cortico-subcortical modulation, might explain these findings.

Aphasia↗

Electrical stimulation of the superior olivary complex can produce cortical evoked potential and behavioral discrimination correlates of pitch perception in the rat.

Patterned electrical stimulation of the superior olivary complex (SOC) which simulated the neural frequency following response (FFR) extracellular potential was used as a stimulus in behavioral frequency discrimination and cortical evoked potential studies. Behavioral judgments of SOC stimulation frequency were found to be as accurate as those obtained for 80 dB acoustic stimuli within the spectral band of the FFR (200 to 3800 Hz). Cortical evoked potentials elicited by acoustic and electrical stimulation of the SOC were then compared for preservation of waveform similarity. Frequency dependent similarity was observed in slow wave events elicited by stimuli with frequencies in the FFR band. A 3 msec time lag was found between acoustic and SOC stimulation produced waveforms which can be accounted for by forward stimulation of the auditory pathway. Our study supports the idea that integrated extracellular waveforms of the FFR index low frequency representations in the auditory brainstem, perhaps by selecting patches of SOC cell transmembrane potential changes. Because bilateral cochlear damage did not prevent behavioral discrimination of SOC electrical stimulation, feedback to the ear is not necessary for perceptual significance of simulated FFR extracellular field potentials in the SOC.

Acoustic Stimulation↗

[Clinical observation of sensorineural hearing loss in patients suffering from nasopharyngeal carcinoma after radiotherapy].

OBJECTIVE: To study the extent and incidence of sensorineural hearing loss (SNHL) after radiotherapy (RT). METHODS: Twenty-eight patients with diagnosed nasopharyngeal carcinoma (NPC) were selected. The pure-tone audiography, auditory brain stem evoked response (ABR), impedance audiometry and evoked otoacoustic emissions (EOAE) recordings were performed before RT, 1 month, 1, 2 and 5 years after RT. RESULTS: At 1 month after RT, there were 7.1 and 25.7 dB increased mean bone conduction (BC) thresholds at speech (0.5 - 4.0 kHz) and at high frequency (8.0 kHz), and their BC thresholds were statistically significant increase than those before RT, respectively (P < 0.001). At 1 year after RT, there were 17.6 and 28.1 dB increased respectively, and their thresholds were statistically significant increase than those at pre-irradiation (P < 0.001). There were also significant increases in thresholds than those at 1 month of post-irradiation (P <0.001 or P < 0.05). At 2 years after RT, 21 and 27.4 dB were increased at respective those two frequencies, and there was a statistically difference only at speech frequencies when compared with those at 1 year after RT (P < 0.05). At 5 years after RT, 26.7 and 35.8 dB were increased at these two frequencies, and there were significant increases in threshold than those before, 1 month, 1 and 2 years after RT, respectively (P < 0.001). From 1 month to 5 years after RT, 37. 5% to 94. 7% of ears had a BC hearing threshold of at least 15 dB losses at speech frequency, whereas the percentage at high frequency was 85.4 to 97.4%. Up to 63.2% and 73.7% of ears had 30 dB SNHL at least at speech and high frequency, respectively. Furthermore, the degree of mean threshold loss was greater at high frequency than at speech frequency. The mean value of wave I, III and V latency, and I -V interpeak latency intervals of ABR had no significant difference between at 1 month after RT and before RT (P > 0.05). The wave I , III and V latency, and I - V interpeak latency intervals at 1 year and 2 years were significantly prolonged when compared with those before and 1 month after RT (P < 0.05), but there were no significant difference between 1 year and 2 years after RT (P > 0.05). The wave I, III and V latency, and I -V interpeak latency intervals at 5 years after RT were also significantly longer than those before RT (P < 0.001). There were significant difference in wave I , III and V latency (P < 0.05), and no significant difference in wave I - V interpeak latency intervals (P > 0. 05) between 5 years after RT and 1 year or 2 years after RT. Seven of 10 ears at 1 year after RT and 4 of 7 ears at 5 years after RT had normal EOAE, but they all had abnormal ABR response. CONCLUSIONS: SNHL in NPC patients start soon after completion of RT, especially more commonly in high frequency. The incidence and the extent of hearing loss are increased with time of follow-up. The hearing impairment could occur in the cochlea and/or the retrocochlear auditory pathway, which show that the sensitivity of radiation damage may be different in different patient and anatomic site of auditory system.

Adult↗

Inferior colliculus stimulation causes similar efferent effects on ipsilateral and contralateral cochlear potentials in the guinea pig.

The inferior colliculus (IC) is a processing center in both the ascending and descending auditory pathways. It has been demonstrated anatomically to send descending projections to the region of the medial olivocochlear (MOC) neurons in the auditory brainstem. Activation of MOC system produces reductions in cochlear neural activity. Individual MOC fibers innervate relatively restricted regions of the cochlea. Recent studies have shown that selective electrical stimulation within the IC central nucleus (ICC) produces frequency-specific reductions of neural activity in the contralateral cochlea (Ota, Y., Oliver, D.L., Dolan, D.F., 2004. Frequency-specific effects on cochlear responses during activation of the inferior colliculus in the guinea pig. J. Neurophysiol. 91, 2185-2193). This efferent effect is likely mediated through selective activation of MOC cells. In this study, we investigated the effects of selective stimulation of one ICC on cochlear output in both ears in anesthetized and paralyzed guinea pigs to explore possible differences in the effective efferent innervation of the two ears. ICC stimulation had a similar tonotopically tuned effect on the distortion product otoacoustic emission (DPOAE) and the cochlear whole-nerve action potential (CAP) in each cochlea. The bandwidth of the efferent effect in each ear was measured and compared at different stimulation levels. For a given ICC stimulation site, the efferent effects were larger for the CAP response. The effect on each response measure was greater in the contralateral than the ipsilateral ear. The effective bandwidth of the efferent effect on the CAP was current-level-dependent but less so for the DPOAE. The results of transections at various locations within the brainstem suggest that the effects were mediated by the MOC system. From the results presented here, the descending efferent system, which originates in the auditory cortex, has frequency-specific, spatially restricted, bilateral effects. The effects are greater in the contralateral ear.

Acoustic Stimulation↗