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Frequency-specific maturation of the eighth nerve and brain-stem auditory pathway: evidence from derived auditory brain-stem responses (ABRs).

Previous studies of human auditory development using frequency-specific auditory brain-stem responses (ABRs) have reported that maturation for both peak and interpeak latencies occurs earlier for responses generated by low-frequency stimuli. In two of these studies, low-frequency ABRs presumed to originate from apical locations in the cochlea were likely dominated by activity from higher frequency regions closer to the base. In the present study, the high-pass noise-masking technique was used to generate derived ABRs that represent activity from isolated place specific regions along the basilar membrane. Analysis of auditory brain-stem maturation based on I-V interpeak latency differences with adult means revealed a frequency-specific pattern of development. Developmental changes occurred faster and mature function was attained earlier for ABRs from the mid-center-frequency (CF) derived conditions than from either the highest or lowest CF derived conditions. The differential maturation of mid-CF derived ABRs may reflect the delayed effects of the pattern of development that occurs in the cochlea.

Auditory Pathways

Effects of aircraft noise on hearing and auditory pathway function of airport employees.

The effects of aircraft noise on hearing and auditory pathway function were studied in 112 airport employees, both by audiometry and brainstem auditory evoked potentials (BAEPs) to evaluate cochlear function and to verify the possibility of retrocochlear involvement. Employees were divided into five groups according to their daily jobs. Group A was made up of 23 maintenance workers, Group B of 20 firemen, Group C of 24 policemen, Group D of 34 airline ground staff, and Group E of 14 civil servants. The typical audiogram pattern of noise-induced hearing loss (NIHL) was a dip at 3 or 4 kHz and moderate hearing loss in the frequency range of 6 to 8 kHz. The results of audiograms in this study revealed the prevalence rate of high-frequency loss in all employees was 41.9%. The incidences of NIHL were highest in the groups of maintenance workers (65.2%) and firemen (55.0%), who are almost continuously exposed to aircraft noise. As for the BAEPs, both click threshold and latencies showed that the impairment was most severe in the groups of maintenance workers and firemen. There was prolongation in central conduction time, shown mainly in intervals of I-V and III-V. This suggests that involvement of the central auditory pathway, especially between the pons and midbrain, is present. In summary, the degree of auditory damage coincided with job patterns. Furthermore, damage of both peripheral cochlear organs and the central auditory pathway by high-frequency aircraft noise exposure was confirmed.

Adult

Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex.

How does cortex that normally processes inputs from one sensory modality respond when provided with input from a different modality? We have addressed such a question with an experimental preparation in which retinal input is routed to the auditory pathway in ferrets. Following neonatal surgical manipulations, a specific population of retinal ganglion cells is induced to innervate the auditory thalamus and provides visual input to cells in auditory cortex (Sur et al., 1988). We have now examined in detail the visual response properties of single cells in primary auditory cortex (A1) of these rewired animals and compared the responses to those in primary visual cortex (V1) of normal animals. Cells in A1 of rewired animals differed from cells in normal V1: they exhibited larger receptive field sizes and poorer visual responsivity, and responded with longer latencies to electrical stimulation of their inputs. However, striking similarities were also found. Like cells in normal V1, A1 cells in rewired animals exhibited orientation and direction selectivity and had simple and complex receptive field organizations. Furthermore, the degree of orientation and directional selectivity as well as the proportions of simple, complex, and nonoriented cells found in A1 and V1 were very similar. These results have significant implications for possible commonalities in intracortical processing circuits between sensory cortices, and for the role of inputs in specifying intracortical circuitry.

Animals

Somatostatin along the auditory pathway.

Several structures associated with the auditory pathway have been examined by radioimmunoassay for their content of somatostatin. Of these, the medial geniculate body had the highest content, followed by the cochlear nucleus, inferior colliculus, auditory cortex and cochlea. Cochlear perilymph had no detectable somatostatin-like immunoreactivity.

Animals

Middle latency auditory evoked potentials improve the detection of abnormalities along auditory pathways in multiple sclerosis patients.

Brain-stem and middle latency auditory evoked potentials (BAEPs and MLAEPs) have been studied in 34 multiple sclerosis (MS) patients. We were able to detect a central nervous system auditory pathway involvement in 17 (50%) of the patients: 38% by BAEPs alone (I-V inter-peak latency) and 47% by MLAEPs alone (Na and Pa peak latency). Five patients had abnormal MLAEPs with normal BAEPs whereas the opposite was detectable in only 1 patient. In addition, most MLAEP parameters in the MS group statistically differed from those obtained in the control group. Therefore, our results demonstrated that the auditory pathway impairment could frequently be located at a rostral level along the auditory radiation. In conclusion, even if only Na and Pa components were considered, MLAEPs succeeded in improving the sensitivity of the auditory evoked potential examination without increasing the false positive rate.

Acoustic Stimulation

Mapping of c-fos expression elicited by pure tones stimulation in the auditory pathways of the rat, with emphasis on the cochlear nucleus.

C-fos expression was mapped in the auditory pathways of rats, stimulated acoustically with pure tones. In the cochlear nucleus, two clusters of c-fos-like immunoreactive neurons, located respectively in the caudal part of the dorsal cochlear nucleus and in the granular cell region, did not show clear systematic shift in their position as a function of the tones frequency. On the other hand, more rostrally in the dorsal cochlear nucleus, a cluster of c-fos-like positive neurons moved progressively from dorsal to ventral for decreasing tones frequency. In the posteroventral cochlear nucleus, another cluster of c-fos-like positive neurons was observed, whose position also varied with tones frequency. Surprisingly, no or very rare c-fos-like immunoreactive neurons were present in the anteroventral cochlear nucleus and in the superior olivary complex. In the inferior colliculus, however, c-fos-like immunoreactive neurons formed clear isofrequency contours, shifting from dorsolateral to ventromedial for increasing tones frequency. In the medial geniculate body c-fos-like immunostaining was restricted to the medial and dorsal divisions while the ventral division was free of labeling. The cause of this differential labeling along the auditory pathways is at present unknown but may eventually provide clues as to physiological differences in parallel auditory pathways.

Acoustic Stimulation

Electrophysiologic assessment of the lower portion of the auditory pathway in the human subject. A preliminary report on auditory evoked eighth nerve and brain stem potentials including their relation to the electrocochleogram.

The electrophysiologic approaches to the assessment of electrical activity of the various portions of the human auditory pathway are reviewed. A method of detection of click evoked eighth nerve and brain stem responses with the use of surface electrodes is described. Preliminary observations in the normal subject with different stimulus parameters and in patients with unilateral deafness are presented. Simultaneous recordings of the eighth nerve and brain stem responses with the cortical evoked response and with the extratympanic electrocochleogram are described. The technique of click evoked eighth nerve and brain stem potentials offers us an additional method of objective assessment of auditory function in a human subject.

Audiometry

The organization of central auditory pathways in a reptile, Iguana iguana.

The present experiments were designed to trace the central auditory pathways in an extant reptile, the New Worlkd lizard--Iguana iguana, utilizing anterograde axonal degeneration stained by the Fink-Heimer ('67) method and the retrograde axonal transport of horseradish peroxidase (LaVail and LaVail, '74). Beginning with the projections of the auditory portion of the VIIIth nerve, the ascending pathways were traced through successive relay nuclei to the telencephalon. The auditory portion of the VIIIth nerve projects to two nuclei in the dorsomedial medulla-nucleus angularis and nucleus magnocellularis medialis. These two nuclei together with a third cll group, nucleus magnocellularis lateralis (intercalated between nucleus angularis and nucleus magnocellularis medialis), have been referred to as the auditory tubercle in previous studies (cf. Miller, '75). The axonal degeneration following large lesions of the auditory tubercle and small lesions of nucleus angularis demonstrated the second order auditory pathways. Fibers leave nucleus angularis ventrally and travel to the ventral surface of the medulla where they cross the midline and ascend to the midbrain in pathways resembling the trapezoid body and the lateral lemniscus of mammals. Along these pathways, terminal arborizations of some fibers were seen in three lower brainstem nuclei while other fibers ascent to the midbrain and terminate in the central nucleus of the torus semicircularis. Experiments in which horseradish peroxidase injections were made in the torus semicircularis demonstrated that nucleus angularis is a primary source of second order auditory fibers to the midbrain and, in addition, that two of the lower brainstem targets of the auditory tubercle project to the torus semicircularis. These lower brainstem pathways were shown to be associated with the auditory system by electrophysiologically recording sound-evoked responses from clusters of cells in the torus semicircularis. Ascending fibers arising from the central nucleus of the torus semicircularis were followed rostrally where they entered the dorsal thalamus and terminated throughout nucleus medialis. Finally, a thalamotelencephalic auditory pathway was traced from nucleus medialis into the lateral forebrain bundle. Terminations of this pathway from nucleus medialis were seen in the medial dorsal ventricular ridge and in the striatum. It was concluded that the ascending auditory pathways of the iguana bear a remarkable resemblance to both the mammalian and avian auditory pathways from the level of the first order neurons in the VIIIth nerve to the level of the telencephalon. At the same time, there are important specializations of the auditory system in birds and mammals such as the development of particular lower brainstem nuclei. Nevertheless, a basic plan for the organization of the auditory system in terrestrial vertebrates can be recognized which invites comparisons with the vertebrate classes that remained in aquatic habitats...

Animals

Frequency selectivity is related to temporal processing in parallel thalamocortical auditory pathways.

Lemniscal and non-lemniscal parallel thalamocortical auditory pathways have been identified with the ventral medial geniculate body (MGB) vs. the dorsal and medial MGB, respectively. Lemniscal neurons have narrow frequency tuning and provide highly specific frequency information to the auditory cortex whereas non-lemniscal neurons generally have broader tuning and greater response lability, including plasticity of frequency receptive fields during learning. To determine if frequency selectivity is related to temporal fidelity of response, we measured both the breadth of tuning and neuronal excitability in a paired tone paradigm for single neurons throughout the MGB. Excitability to the second tone of a pair was directly correlated with frequency selectivity: the narrower the frequency tuning, the greater the excitability. Cells with broad tuning based on multiple-peak response areas also were less excitable than cells with single-peak RAs. Cells in the ventral MGB showed greater temporal fidelity of response (greater excitability) than cells in the dorsal and medial MGB. These findings show that high degrees of both frequency selectivity and temporal response fidelity are characteristic of the lemniscal, but not the non-lemniscal, thalamocortical auditory system.

Acoustic Stimulation

Development of the brainstem auditory pathway in low birthweight and perinatally asphyxiated children with neurological sequelae.

Low birthweight (LBW) and perinatal asphyxia are known to be high-risk factors for a number of neurodevelopmental deficits. In this study, we analyzed brainstem auditory evoked response (BAER) in 18 LBW and 36 perinatally asphyxiated children with non-progressive neurological sequelae after the age of 6 months to inspect and compare the long-term influence of LBW and perinatal asphyxia on the brainstem auditory pathway. The typical changes in the BAER of children born with LBW were slightly shorter III-V interpeak interval and smaller III-V/I-III interval ratio than normal controls. On the contrary, the abnormalities in the BAER of 36 children surviving perinatal asphyxia were characterized by a reduction of the amplitude of wave V with normal intervals. This discrepancy in the BAER between the children born with LBW and those with perinatal asphyxia implies that the two high-risk factors exert different long-term influences on the development of the brainstem auditory pathway. It is hypothesized that these characteristic changes may be indicative of a major influence of LBW on the generators contributing to wave III and that of asphyxia on the generators contributing to wave V. An increase in response threshold with abnormal latency-intensity function was found in 11% of the LBW children and 19% of the asphyxiated children, suggesting that sensorineural hearing impairment occurred more frequently in children surviving perinatal asphyxia than in those born with LBW. Follow-up study demonstrates that the abnormalities in the brainstem auditory pathway of LBW and asphyxiated children after the age of 6 months is likely to be persistent.

Asphyxia Neonatorum

Organization of the auditory pathway in the thoracic ganglia of noctuid moths.

We describe the neuroarchitecture of the noctuid thoracic nerve cord and use this framework to interpret the organization of the auditory pathway responsible for escape behaviour in noctuid moths. Noctuid moths possess only two auditory receptors (A1, A2), in each ear. The axon of the A1 cell projects initially to a glomerulus located ventrally and medially in the metathoracic ganglion, where it bifurcates. One branch ascends in the ventral intermediate tract to the brain, the other descends in the ventral intermediate tract into abdominal neuromeres of the metathoracic ganglion. Both axons arborize in the median ventral and ring tracts in each neuromere. The central projections of the A2 cell remain largely within the metathoracic ganglion. The axon bifurcates at the midline and directs arborizations dorsally to the dorsal intermediate and median dorsal tracts, and ventrally into the ring tract where the arborizations overlap those of the A1 afferent. The afferent projections remain ipsilateral to the ear of origin. We describe a posterior auditory association area in the metathoracic ganglion in which the major arborizations of several identified interneurones overlap those of the A1 afferent and make monosynaptic connections with it. These interneurones all respond tonically to sound stimuli. We have also identified the projections of the A1 afferent, interneurones, and motor neurones in the segmentally equivalent anterior auditory association area of the mesothoracic ganglion. An interneurone with major arborizations in the same tracts as the A1 afferent, and receiving monosynaptic input from it, is described. The arborizations of higher order interneurones lie mainly in dorsal tracts along with those of flight motor neurones. All the interneurones in this anterior centre respond phasically or phasic/tonically to sound stimuli. The relevance of this anatomical organization for predator avoidance behaviour is considered and the organization of auditory pathways in tympanate insects compared.

Animals

[Characteristics of the reactions of neurons of successive links in the auditory pathway to changes in the timing of acoustic signals].

Afferent impulsation was compared for different levels of the auditory system: the cochlear nuclei, posterior colliculi, and the auditory cortex. While moving from the cochlear nuclei over to the posterior colliculi and the auditory cortex, the number of neurons describing the temporal structure of the amplitude-modulated signal's envelope in the impulse activity pattern, becomes sharply reduced; the number of neurons selectively responding to certain phases of the envelope increases; the firing rate of neurons of the auditory pathway's higher levels decreases; the repetition rates becomes narrow due to limitation from both the high- and the low-frequency sides. Selectivity of responses to combination of such signal parameters as the frequency of the carrier and the rhythm of the amplitude modulation, increases. Specificity of the neuronal responses increases on certain combinations of such parameters of the frequency-modulated sounds as the frequency range in the signal, the direction and speed of the frequency modulation. The data obtained revealed some general tendencies of the impulsation transformation in successive levels of the auditory pathway.

Animals

GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats.

A comparative study of the immunostain to antibodies directed against glutamic acid decarboxylase (GAD) and gamma-aminobutyric acid (GABA) in the ascending auditory pathway was carried out in horseshoe bats (Rhinolophus rouxi) and mustached bats (Pteronotus parnellii). In both species GAD/GABA-positive puncta (presumed axonal boutons) and GAD/GABA-positive cells were found in the cochlear nucleus, the superior olivary complex, the nuclei of the lateral lemniscus the inferior colliculus, and the medial geniculate body. General features of the immunostaining pattern in the auditory pathway agree with observations in other mammals. Quantitative analysis of puncta distribution shows that many auditory centers are characterized by subregional differences in puncta density and distribution. This indicates local differences in putatively inhibitory input related to connectivity and tonotopic organization. The following species characteristic features were found: 1) The dorsal non-laminated portion of the dorsal cochlear nucleus in horseshoe bats lacks the GAD/GABA-immunoreactive cells typical for the ventral laminated portion and the dorsal cochlear nucleus of other species. Clearly, a cytoarchitectonic specialization is accompanied by a loss of putatively GABAergic local inhibitory circuits. 2) The ventral division of the medial geniculate body of the mustached bat lacks GAD/GABA-immunopositive cells. Such cells are present in the horseshoe bat and other mammals. This finding implies functional differences in the organization of the medial geniculate body within the same mammalian order.

Animals

[Influence of acoustic stimulation in the maturation of the auditory pathway].

The aim of this study is to analyze the relationship between age and the maturational changes occurring in the peripherical auditory system and the influence of the acoustic stimulation. With this purpose Auditory Brainstem Responses (ABR) were recorded at the 35 and 39 weeks gestational age, in 56 ears of 28 premature infants. The ABR were analyzed the changes in latency values of the I, V waves and I-V intervals. In order to know the influence of the acoustic stimulation on the development of auditory pathway, we made 2 groups with the 28 premature children, one of them control group and the other stimulated with maternal voice from 35 till 39 weeks. The stimulated group had one maturate auditory evoked responses at 39 weeks gestational age. Showing a latency decrease wave V and I-V interval, compared to control group.

Acoustic Stimulation

Auditory pathways to the cortex in Tupaia glis.

The auditory system of the tree shrew, Tupaia glis, was investigated by identifying axonal degeneration after lesions of the lateral lemniscus, the inferior colliculus, the medial geniculate nucleus and the auditory cortex. The results show that the lateral lemniscus projects to the central nucleus of the inferior colliculus which in turn projects principally to the ventral division of the medial geniculate nucleus but to a lesser extent to the magnocellular division of the medial geniculate nucleus. The final step in the pathway to the cortex is achieved by a projection from the ventral division to the fourth layer of auditory koniocortex. There appear to be several auditory pathways parallel to this primary path. The lateral lemniscus projects to the dorsal division of the medial geniculate nucleus; the deeper layers of the superior colliculus project to the posterior nucleus; and both the dorsal division and the posterior nucleus project to the belt caudal to auditory koniocortex. The caudal division of the medial geniculate nucleus may constitute a relay in still another path from the pericentral division of the inferior colliculus. Finally, the magnocellular division also appears to be distinct insofar as its cortical projections are confined chiefly to the deeper layers. A comparison between the tree shrew and the cat reveals a similar organization in the two species. In the cat the starting point for understanding the organization of the several auditory pathways is the distinction between a core cortical zone which corresponds to konicortex and to AI and a peripheral belt. The core receives essential projections from the ventral division; the belt receives sustaining projections from the cell groups which surround the ventral division. It is reasonable to hypothesize that this difference between the core and the belt is characteristic of all mammals.

Animals

Visual projections induced into the auditory pathway of ferrets. I. Novel inputs to primary auditory cortex (AI) from the LP/pulvinar complex and the topography of the MGN-AI projection.

The organization of cortical circuitry responsible for processing sensory information is a subject of intense examination. However, it is not known whether cortical cells in different sensory cortices process information in a way that is specific to the modality of their input, or whether there are commonalities in processing circuitry across different cortices. In our laboratory, this question has been investigated at the level of the geniculocortical pathway by routing information of one sensory modality into the processing circuitry of another modality. Appropriate early lesions cause growth of retinal axons into the auditory thalamus (MGN) (Sur et al., Science 242:1437, '88). Previously, we have established that the MGN carries the resulting visual information on to primary auditory cortex (AI), which thus contains visually responsive neurons and a topographic representation of the retina (Roe et al., Soc. Neurosci. Abstr. 14:460, '88; Sur et al., Science 242:1437, '88). In this paper, we describe anomalous projections from the dorsal part of the thalamus, specifically the lateral posterior/pulvinar complex, into AI. This result demonstrates that thalamic neurons belonging to one modality can be induced to project to cortex that is normally of a different modality. In addition, we have studied in detail the nature of the MGN to AI projection in these animals as compared to the normal projection. The MGN to AI projection appears to be unaltered by the lesions; the location and topography of labelled cells are similar to that in normal animals. Because the MGN to AI projection is still highly divergent along the "isofrequency" dimension when compared to the tonotopic dimension, our data suggest that visual topography in the cortical map is created within the auditory cortex, perhaps by activity-dependent sharpening of the retinal representation during development.

Animals