Auditory Afferents Research Articles

Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons.

This paper reports on directional response properties of saccular afferents of the sleeper goby, Dormitator latifrons, to 100-Hz acoustic particle motions with a focus on testing the hypothesis that the response directionality of a fish's auditory afferents derives from the morphological polarity of sensory hair cells in the otolithic organs. Spontaneous rates (SR) and best sensitivities (BS) of saccular afferents ranged from 0 to 162 spikes/sec and from 0.2-to 100-nm RMS displacement. SR did not vary with BS. Most saccular afferents were phase-locked to sinusoidal stimulation and had sustained temporal response patterns with some adaptation. All saccular afferents were directionally sensitive to the stimulus, and the sharpness of directional response curves was determined by a directionality index (DI). The DI ranged from 0.64 to 1.50 (mean = 1.02, SE = 0.02, n = 100) and gradually decreased with stimulus level throughout afferents' response dynamic range. Many afferents had approximately symmetric directional response curves relative to their best response axes (BRA). BRA of most afferents remained constant with stimulus level. The BRA distribution had a peak along an axis that correlates closely with the morphological polarity of saccular hair cells. Therefore, our results strongly support the hypothesis.

A model for prelingual deafness, the congenitally deaf white cat – population statistics and degenerative changes

Cochlear implantation in congenitally deaf children leads to electrical stimulation of an entirely naive central auditory system. In this case, processes of central auditory maturation are induced by the electric stimuli. For the study of these processes the deaf white cat (DWC) appears to be an appropriate model. However, a knowledge of the basic data of these animals is necessary before such a model may be used. This paper presents these data and is one of a series of publications concerning congenital deafness in children and cochlear implantation. In our strain 72% of the animals are totally deaf as judged by the absence of any brain stem evoked potentials at click intensities up to 120 dB SPL peak equivalent. Primarily, there is a degeneration of the entire organ of Corti during the first postnatal weeks. An absence of acoustically evoked brain stem responses in the early postnatal weeks shows that DWCs probably never have any hearing experience. Months after the degeneration of the organ of Corti, the spiral ganglion starts to degenerate from the midportion of the cochlea. However, even in adult cats (2 years), a sufficient number of functionally intact auditory afferents remain, which are suitable for electrical cochlear stimulation.

A fast synaptic potential mediated by NMDA and non-NMDA receptors.

A fast synaptic potential mediated by NMDA and non-NMDA receptors. J. Neurophysiol. 78: 2693-2706, 1997. Excitatory synaptic transmission in the CNS often is mediated by two kinetically distinct glutamate receptor subtypes that frequently are colocalized, the N-methyl--aspartate (NMDA) and non-NMDA receptors. Their synaptic currents are typically very slow and very fast, respectively. We examined the pharmacological and physiological properties of chemical excitatory transmission at the mixed electrical and chemical synapses between auditory afferents and the goldfish Mauthner cell, in vivo. Previous physiological data have suggested the involvement of glutamate receptors in this fast excitatory postsynaptic potential (EPSP), the chemical component of which decays with a time constant of <2 ms. We demonstrate here that the pharmacological and voltage-dependent characteristics of the synaptic currents are consistent with glutamatergic transmission and that both NMDA and non-NMDA receptors are involved. The two components surprisingly exhibit quite similar kinetics even at resting potential, with the NMDA response being only slightly slower. Due to its fast kinetics and characteristic voltage dependence, NMDA receptor-mediated transmission at these first-order synapses contributes significantly to paired pulse and frequency-dependent facilitation of successive fast EPSPs during high-frequency repetitive firing, a presynaptic impulse pattern that induces activity-dependent homosynaptic changes in both electrical and chemical transmission. Thus NMDA receptor kinetics in this intact preparation are suited to its functional requirements, namely speed of information transmission and the ability to trigger changes in synaptic efficacy.

Afferent and efferent connections of the ventrolateral tegmental area in the rat.

The present study examined the organization of afferent and efferent connections of the rat ventrolateral tegmental area (VLTg) by employing the retrograde and anterograde axonal transport of Fluorogold and Phaseolus vulgaris-leucoagglutinin, respectively. Our interest was focused on whether the anatomical connections of the VLTg would provide evidence as to the involvement of this reticular area in audiomotor behavior. Our retrograde experiments revealed that minor inputs to the VLTg arise in various telencephalic structures, including the cerebral cortex. Stronger projections originate in the lateral preoptic area, the zona incerta, the nucleus of the posterior commissure and some other thalamic areas, the lateral substantia nigra, the deep layers of the superior colliculus, the dorsal and lateral central gray, the deep mesencephalic nucleus, the paralemniscal zone, the intercollicular nucleus, the external cortex of the inferior colliculus, the oral and caudal pontine reticular nucleus, the deep cerebellar nuclei, the gigantocellular and lateral paragigantocellular reticular nuclei, the prepositus hypoglossal nucleus, the spinal trigeminal nuclei, and the intermediate layers of the spinal cord. Most importantly, we disclosed strong auditory afferents arising in the dorsal and ventral cochlear nuclei and in the cochlear root nucleus. The efferent projections of the VLTg were found to be less widespread. Telencephalic structures do not receive any input from the VLTg. Moderate projections were seen to diencephalic reticular areas, the zona incerta, the nucleus of the posterior commissure, and to various other thalamic areas. The major VLTg projections terminate in the deep layers of the superior colliculus, the deep mesencephalic nucleus, the intercollicular nucleus and external cortex of the inferior colliculus, the oral and caudal pontine reticular nucleus, the gigantocellular and lateral paragigantocellular reticular nuclei, and in the medial column of the facial nucleus. From our data, we conclude that the VLTg might play a role in sensorimotor behavior.

Neuronal basis of phonotactic behaviour in Tettigonia viridissima ?: processing of behaviourally relevant signals by auditory afferents and thoracic interneurons

Information transmission in the auditory pathway of Tettigonia viridissima was investigated using song models and artificial stimuli. Receptor cells respond tonically to song models and copy the syllable pattern within a wide intensity range. The omega-neuron responds tonically to soma-ipsilateral stimuli. Contralateral stimuli elicit IPSPs both within dendritic (ipsilateral) and axonal (contralateral) branches, thereby emphasizing directionality. Both AN1 and AN2 respond with tonic, non-adapting responses, precisely copying the syllable pattern of the song. While AN1 is excited by sonic frequencies and inhibited by ultrasonic frequencies, AN2 responds predominantly to ultrasound. The TN1 only responds to the ultrasonic components of the song, with phasic responses, which adapt quickly. In the adapted state, it responds selectively to the time pattern of the conspecific song, but not to the song patterns of two syntopic Tettigonia species. TN2, which has not been described up until now, is tuned to ultrasonic frequencies. Its responses to song models vanish after a few syllables, because of quick adaptation. The morphology is unusual with the axon running contralateral to the input site. The behavioural relevance of auditory interneurons is discussed and compared with the auditory system of crickets.

Frequency representation in the emu basilar papilla

The frequency representation on the basilar papilla of the emu was investigated by recording from single auditory afferents and labeling them iontophoretically with horseradish peroxidase. Successfully labeled fibers covered a range of characteristic frequencies from 0.05 to 3.3 kHz, which corresponded to nearly 90% of the total papillar length. The termination sites of labeled fibers within the basilar papilla correlated with their characteristic frequency, the lowest frequencies being represented apically, the highest basally. The best mathematical description of the frequency distribution was given by an exponential regression, with a uniform mapping constant of 0.8 mm/octave. This function deviates from the more commonly observed pattern of increasing space constant towards higher frequencies. Most labeled fibers innervated only one hair cell; those contacting 4 or more hair cells were all of low characteristic frequency (⩽0.11 kHz). All labeled fibers terminated within the neural 56% of the basilar papilla’s width. This innervation pattern is consistent with that observed in other bird species. There was no conclusive evidence for a change of sensitivity and/or frequency selectivity with innervational position across the papilla’s width.

Behavioral response to ultrasound by the tiger beetle Cicindela marutha dow combines aerodynamic changes and sound production.

Tethered flying tiger beetles, Cicindela marutha, respond to trains of bat-like ultrasonic pulses with a short-latency, multi-component behavior. The head rolls to one side, the metathoracic legs kick to the opposite side, the elytra swing backwards towards the hindwings and pronate, the hindwings increase their stroke excursion and frequency, and the plane of the hindwing motion tilts forward. In addition, the beetles produce trains of ultrasonic clicks typically containing 100-200 clicks in response to a 1 s stimulus. The clicks average 85-90 dB SPL at 2 cm. The latencies for hindwing changes and elytra swing in response to stimuli more than 10 dB over threshold are 90-110 ms; the latency to clicking is 120-150 ms. Neither the head roll nor the leg kick appears to be directional relative to the sound source. The behavioral response is broadly tuned with greatest sensitivity at 30-60 kHz and mean behavioral thresholds of 75-80 dB SPL. Physiological audiograms from the auditory afferents show substantially greater sensitivity and sharper tuning than the behavioral response, which suggests that tiger beetles may use their hearing in other contexts as well as during flight. The combination of aerodynamic components and arctiid-month-like clicking may provide these insects with a powerful defense against attack by echolocating bats.

The number of primary auditory afferents in the rat

Published estimates of the number of primary auditory afferents in the rat differ by as much as 30%. We undertook to determine if the widely varying estimates were related to methodological differences, especially the difference between counting cells in Rosenthal's canal and fibers in the cochlear nerve. Type I ganglion cells and myelinated cochlear nerve fibers in the same ears were counted in Long-Evans and Sprague-Dawley strains. Type II spiral ganglion cells were also counted. In each strain the numbers of myelinated fibers and type I ganglion cells were essentially the same. Means for the Long-Evans were 18,036 fibers and 17,749 cells. Means for Sprague-Dawleys were higher: 19,444 fibers and 19,229 cells. The mean number of type II ganglion cells was also greater in Sprague-Dawley than in Long-Evans rats: 1,388 and 1,170, respectively. Cell and fiber counts from the two ears of the same animal differed on average by only 1%. The number of auditory afferents did not change with age over the range (2–10 months) studied here. Several methodological differences have probably contributed to the varying estimates of type I primary auditory afferents, but the discrepancies are not inherent in counts of fibers and spiral ganglion cells.

Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea.

Sound localization is a basic processing task of the auditory system. The directional detection of an incident sound impinging on the ears relies on two acoustic cues: interaural amplitude and interaural time differences. In small animals, with short interaural distances both amplitude and time cues can become very small, challenging the directional sensitivity of the auditory system. The ears of a parasitoid fly Ormia ochracea, are unusual in that both acoustic sensors are separated by only 520 microns and are contained within an undivided air-filled chamber. This anatomy results in minuscule differences in interaural time cues (ca. 2 microseconds) and no measurable difference in interaural intensity cues generated from an incident sound wave. The tympana of both ears are anatomically coupled by a cuticular bridge. This bridge also mechanically couples the tympanana, providing a basis for directional sensitivity. Using laser vibrometry, it is shown that the mechanical response of the tympanal membranes has a pronounced directional sensitivity. Interaural time and intensity differences in the mechanical response of the ears are significantly larger than those available in the acoustic field. The tympanal membranes vibrate with amplitude differences of about 12 dB and time differences on the order of 50 microseconds to sounds at 90 degrees off the longitudinal body axis. The analysis of the deflection shapes of the tympanal vibrations shows that the interaural differences in the mechanical response are due to the dynamic properties of the tympanal system and reflect its intrinsic sensitivity to the direction of a sound source. Using probe microphones and extracellular recording techniques, we show that the primary auditory afferents encode sound direction with a time delay of about 300 microseconds. Our data point to a novel mechanism for directional hearing in O. ochracea based on intertympanal mechanical coupling, a process that amplifies small acoustic cues into interaural time and amplitude differences that can be reliably processed at the neural level. An intuitive description of the mechanism is proposed using a simple mechanical model in which the ears are coupled through a flexible lever.

Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents

Natural sounds, especially communication sounds, have highly structured amplitude and phase spectra. We have quantified how structure in the amplitude spectrum of natural sounds affects coding in primary auditory afferents. Auditory afferents encode stimuli with naturalistic amplitude spectra dramatically better than broad-band stimuli (approximating white noise); the rate at which the spike train carries information about the stimulus is 2-6 times higher for naturalistic sounds. Furthermore, the information rates can reach 90% of the fundamental limit to information transmission set by the statistics of the spike response. These results indicate that the coding strategy of the auditory nerve is matched to the structure of natural sounds; this 'tuning' allows afferent spike trains to provide higher processing centres with a more complete description of the sensory world.

The neural mechanism for directional escape in the goldfish

In response to sudden sound, many fishes rapidly accelerate away from the stimulus. This complex behavior, or C-start, is mediated by a network of brain-stem neurons that receive acoustic input and connect to motoneurons in the spinal cord. In the brain-stem network, the bilateral pair of Mauthner cells (M-cells) play the major role in determining the initial direction of the C-start. Each M-cell axon crosses the brain and connects to motoneurons on the opposite side of the body, so that the animal turns away from the side of the activated M-cell. M-cells receive primary acoustic afferents and inhibitory input from a network of ‘‘PHP’’ cells. PHP cells have a very short latency response to sound and operate in a feedforward mode to regulate M-cell firing threshold. These studies suggest that the PHP cells receive specific combinations of pressure- and displacement-sensitive auditory afferents that inhibit the M-cell to sounds coming from the side of the body opposite the stimulus. Thus only the correct M-cell fires, while its opposite counterpart is inhibited by PHP cells. Present studies involve an electrophysiological, behavioral, and neurocomputational analysis of this hypothesis. [Work supported by NIH and ONR.]

Increasing background inspiratory resistance changes somatosensory sensations in healthy man

The central purpose of the study was to investigate if increasing background inspiratory resistance, a circumstance which activated afferents from the lungs and respiratory muscles, modified somatosensory and/or auditory sensations in healthy individuals. Estimation of mechanical stimulations applied on the middle finger (somatosensory sensation) and unilateral sound-pressure stimulations (auditory sensation) was based on the computation of Stevens' power function ψ = k./ gf n, where ψ is the estimate and /gf is either the somatonsensory stimuli or sound-pressures. This was studied during eupnoeic unloaded ventilation then during a 10-min period of loaded breathing followed by a 10-min recovery period. Loaded breathing significantly lowered the estimate of somatosensory stimuli (decreased n coefficient). This effect persisted during the two first minutes of recovery period. By contrast, loaded breathing did not modify the perception of auditory stimulus. As somesthetic and respiratory afferents, but not auditory afferents, project on the same area in the sensory cortex we suggest the existence of central interactions which could explain clinical observations of the difficulties to execute accurate tasks in patients suffering from obstructive lung disease independently from the alterations in their arterial blood gases.

Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell

Large myelinated club endings of the goldfish eighth nerve arise in the sacculus and establish mixed electrotonic and chemical synapses with the distal part of the Mauthner (M-) cell's lateral dendrite. We show here, using paired pre- and postsynaptic recordings, that depolarizing currents generated postsynaptically (specifically, the mixed synaptic potential produced by activation of part of the afferent population) can in some cases excite the presynaptic fibers and cause them to backfire. Strikingly, while in some systems junctional properties prevent the antidromic spread of depolarizing currents, physiological properties of these afferents and the gap junctions promote backfiring: the amplitude of the coupling potential recorded from an afferent fiber is voltage dependent, increasing with depolarization and being reduced during hyperpolarization. Two mechanisms, with different kinetics, underlie this voltage dependence. One, a nonlinear membrane property of the afferent fiber itself, enhances the coupling potential as the afferent membrane depolarizes. The second mechanism, which is less sensitive to voltage and is symmetric about the resting potential, most likely represents voltage dependence of the junctional membrane. Additionally, we also show retrograde diffusion of low molecular weight substances, as the fluorescent dye Lucifer yellow and the tracer Neurobiotin were found in the terminals of afferent fibers after being injected postsynaptically into the M-cell. These results suggest that the gap junctions in these primary afferents are not only involved in fast anterograde synaptic transmission but also provide the substrate for a retrograde intercellular communication. The electrical coupling may modify the input-output relation between eighth nerve afferents and the lateral dendrite by synchronizing the population of already active fibers and by promoting the recruitment of new fibers via backfiring, such that weaker inputs produce relatively larger responses.

Characterization of auditory afferents in the tiger beetle, Cicindela marutha Dow

We have identified a nerve carrying auditory afferents and characterized their physiological responses in the tiger beetle, Cicindela marutha. 1. The tympana are located at the lateral margins of the first abdominal tergum. The nerve carrying the tympanal afferents is a branch of the dorsal root from the first abdominal ganglion. 2. Both male and female auditory afferent responses are sharply tuned to 30 kHz with sensitivities of 50-55 dB SPL. 3. The auditory afferents show little adaptation and accurately code the temporal characteristics of the stimulus with the limit of a resolution of 6-10 ms. 4. The difference in threshold between contralateral and ipsilateral afferents for lateral stimuli is greatest at 30 kHz and is at least 10-15 dB. 5. Ablation studies indicate that the floppy membrane in the anterolateral corner of the tympanum is crucial for transduction while the medial portion of the tympanum is less important. 6. The tiger beetle and acridid (locust and grasshopper) ears have evolved independently from homologous peripheral structures. The neural precursor of the tympanal organs in both animals is likely the pleural chordotonal organ of the first abdominal segment.

A common neural code for frequency- and amplitude-modulated sounds.

Most naturally occurring sounds are modulated in amplitude or frequency; important examples include animal vocalizations and species-specific communication signals in mammals, insects, reptiles, birds and amphibians. Deciphering the information from amplitude-modulated (AM) sounds is a well-understood process, requiring a phase locking of primary auditory afferents to the modulation envelopes. The mechanism for decoding frequency modulation (FM) is not as clear because the FM envelope is flat (Fig. 1). One biological solution is to monitor amplitude fluctuations in frequency-tuned cochlear filters as the instantaneous frequency of the FM sweeps through the passband of these filters. This view postulates an FM-to-AM transduction whereby a change in frequency is transmitted as a change in amplitude. This is an appealing idea because, if such transduction occurs early in the auditory pathway, it provides a neurally economical solution to how the auditory system encodes these important sounds. Here we illustrate that an FM and AM sound must be transformed into a common neural code in the brain stem. Observers can accurately determine if the phase of an FM presented to one ear is leading or lagging, by only a fraction of a millisecond, the phase of an AM presented to the other ear. A single intracranial image is perceived, the spatial position of which is a function of this phase difference.

Autoradiographic labelling of P 2 purinoceptors in the guinea-pig cochlea

Two different radioligands were used to identify extracellular ATP binding sites specific to P 2 purinoceptors in guinea-pig cochlear tissue. Deoxyadenosine 5′-(α-[ 35S]thio)triphosphate ([ 35S]dATPαS; 10 nM) provided a high activity probe for the P 2y purinoceptor subtype on the basis of selective block by 2-methylthio-ATP (2MeSATP; 100 μM). [ 3H]α,β-methylene-ATP (10 nM), a high affinity probe for a P 2x purinoceptor subtype was selectively blocked by inclusion of the related compound β,γ-methylene-ATP (100 μM). Both probes labelled the organ of Corti, stria vascularis and spiral prominence regions. The P 2x purinoceptor probe also bound to lateral wall tissue below the spiral prominence and insertion point of the basilar membrane within the scala tympani compartment, a region which failed to show significant binding using [ 35S]dATPαS. Frozen sections of whole cochlea permitted analysis of radioligand binding to the cell body region (spiral ganglion in Rosenthal's canal) of the primary auditory afferents and the auditory nerve itself, which lies within the central region of the modiolus of the cochlea. Both these regions exhibited 2MeSATP blockable [ 35S]dATPαS binding whereas specific [ 3H]α,β-methylene-ATP binding was absent from spiral ganglion and minimal in the auditory nerve region. These results demonstrate a mixed P 2 purinoceptor distribution in cochlear tissues and suggest that complex purine-mediated neurohumoral mechanisms may influence cochlear function at a number of sites.

Rate-intensity-functions of pigeon auditory primary afferents

Rate-intensity-functions (RI-functions) were determined in 150 primary auditory afferents in anaesthetized pigeon. Acoustic stimulation was either at characteristic frequency (CF) or half an octave below or above CF. Stimulated at CF, 37% of the fibres showed saturating RI-functions, whereas 50% showed sloping and 13% straight RI-functions. In the sloping RI-functions, a bend was found about 20 dB above the fibres' thresholds. For non-CF stimuli, the general shape of the RI-functions remained constant. However, the maximum evoked discharge rates were lower for frequencies below CF and higher for frequencies above CF. The data show that a population of neurones, the sloping and straight ones, code stimulus intensities over a wide intensity range. In combination with the scatter of the thresholds, intensity ranges greater than 100 dB are conceivable. It was concluded that the nonlinearities found in pigeon are not caused by basilar membrane (BM) mechanics, rather an origin at the hair cell-afferent nerve fibre system has to be considered.

Characterization of auditory afferents in the tiger beetle,Cicindela marutha Dow

Characterization of auditory afferents in the tiger beetle,Cicindela marutha Dow

Preferred intervals in birds and mammals: A filter response to noise?

Quasi-periodic spontaneous activity (preferred intervals, PIs) has been reported from avian primary auditory afferents. In mammals, PIs have not been reported, as yet. As the length of PIs is close to 1/characteristic frequency, it has been suggested that this type of spontaneous activity indicates particular mechanisms in avian inner ear transduction. However, the present paper shows that pigeon auditory fibres possessing preferred intervals in their spontaneous activity always belong to the most sensitive and the most sharply-tuned fibres recorded. This leads to the assumption that preferred intervals are the response of narrow-band filters to noise. This view is supported by three additional findings: (i) Near-threshold noise provokes PIs in avian fibres that show no spontaneous PIs. (ii) Similarly, PIs can also be evoked in mammalian (gerbil) auditory afferents by low level noise, (iii) Phase-locking of auditory afferents can be achieved by sound stimuli 10–20 dB below rate threshold. It is argued that no conclusions may be drawn from the presence of PIs about the nature of the underlying filter.

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears. The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.