Tails Of Tuning Curves Research Articles

In vivo Whole-Cell Recordings Combined with Electron Microscopy Reveal Unexpected Morphological and Physiological Properties in the Lateral Nucleus of the Trapezoid Body in the Auditory Brainstem.

The lateral nucleus of the trapezoid body (LNTB) is a prominent nucleus in the superior olivary complex in mammals including humans. Its physiology in vivo is poorly understood due to a paucity of recordings. It is thought to provide a glycinergic projection to the medial superior olive (MSO) with an important role in binaural processing and sound localization. We combined in vivo patch clamp recordings with labeling of individual neurons in the Mongolian gerbil. Labeling of the recorded neurons allowed us to relate physiological properties to anatomy at the light and electron microscopic level. We identified a population of quite dorsally located neurons with surprisingly large dendritic trees on which most of the synaptic input impinges. In most neurons, one or more of these dendrites run through and are then medial to the MSO. These neurons were often binaural and could even show sensitivity to interaural time differences (ITDs) of stimulus fine structure or envelope. Moreover, a subpopulation showed enhanced phase-locking to tones delivered in the tuning curve tail. We propose that these neurons constitute the gerbil main LNTB (mLNTB). In contrast, a smaller sample of neurons was identified that was located more ventrally and that we designate to be in posteroventral LNTB (pvLNTB). These cells receive large somatic excitatory terminals from globular bushy cells. We also identified previously undescribed synaptic inputs from the lateral superior olive. pvLNTB neurons are usually monaural, display a primary-like-with-notch response to ipsilateral short tones at CF and can phase-lock to low frequency tones. We conclude that mLNTB contains a population of neurons with extended dendritic trees where most of the synaptic input is found, that can show enhanced phase-locking and sensitivity to ITD. pvLNTB cells, presumed to provide glycinergic input to the MSO, get large somatic globular bushy synaptic inputs and are typically monaural with short tone responses similar to their primary input from the cochlear nucleus.

Modeling disrupted tonotopicity of temporal coding following sensorineural hearing loss

Perceptual studies suggest that sensorineural hearing loss (SNHL) affects neural coding of temporal fine structure (TFS) more than envelope (ENV). Although the “quantity” of TFS coding is degraded only in background noise, Wiener-kernel analyses suggest SNHL disrupts tonotopicity (i.e., the “quality”) of TFS coding for complex sounds more than ENV coding. Specifically, auditory-nerve (AN) fibers in noise-exposed chinchillas can have their dominant TFS component located within their tuning-curve tail (i.e., the wrong place) while their ENV response remains centered at CF. Here, the ability of a AN model [Zilany and Bruce (2007)] to replicate this dissociation between TFS and ENV tonotopicity was evaluated. By varying the degree of outer- and inner-hair-cell damage, hypothesized factors such as hypersensitive tails and tip-to-tail ratio were evaluated. The model predicted the main trends in our physiological data: (1) no loss of tonotopicity for lower CFs without a clear tip/tail distinction, (2) more easily disrupted TFS tonotopicity than ENV (without requiring hypersensitive tails), and (3) disruption of both TFS and ENV tonotopicity for severely degraded tips. This computational approach allows exploration of the interaction between tip-tail ratio and phase-locking roll-off, and whether amplification strategies can restore cochlear tonotopicity. [Work supported by NIH grants R01-DC009838 and F32-DC012236.]

Medial efferent effects on auditory-nerve responses to tail-frequency tones II: alteration of phase.

It is often assumed that at frequencies in the tuning-curve tail there is a passive, constant coupling of basilar-membrane motion to inner hair cell (IHC) stereocilia. This paper shows changes in the phase of auditory-nerve-fiber (ANF) responses to tail-frequency tones and calls into question whether basilar-membrane-to-IHC coupling is constant. In cat ANFs with characteristic frequencies > or = 10 kHz, efferent effects on the phase of ANF responses to tail-frequency tones were measured. Efferent stimulation caused substantial changes in ANF phase (deltaphi) (range -80 degrees to +60 degrees, average -15 degrees, a phase lag) with the largest changes at sound levels near threshold and 3-4 octaves below characteristic frequency (CF). At these tail frequencies, efferent stimulation had much less effect on the phase of the cochlear microphonic (CM) than on ANF phase. Thus, since CM is synchronous with basilar-membrane motion for low-frequency stimuli in the cochlear base, the efferent-induced change in ANF phase is unlikely to be due entirely to a change in basilar-membrane phase. At tail frequencies, ANF phase changed with sound level (often by 90 degrees-180 degrees) and the deltaphi from a fiber was positively correlated with the slope of its phase-versus-sound-level function at the same frequency, as if deltaphi were caused by a 2-4 dB increase in sound level. This correlation suggests that the processes that produce the change in ANF phase with sound level at tail frequencies are also involved in producing deltaphi. It is hypothesized that both efferent stimulation and increases in sound level produce similar phase changes because they both produce a similar mix of cochlear vibrational modes.

Medial efferent effects on auditory-nerve responses to tail-frequency tones. I. Rate reduction

One way medial efferents are thought to inhibit responses of auditory-nerve fibers (ANFs) is by reducing the gain of the cochlear amplifier thereby reducing motion of the basilar membrane. If this is the only mechanism of medial efferent inhibition, then medial efferents would not be expected to inhibit responses where the cochlear amplifier has little effect, i.e., at sound frequencies in the tails of tuning curves. Inhibition at tail frequencies was tested for by obtaining randomized rate-level functions from cat ANFs with high characteristic frequencies (CF > or = 5 kHz), stimulated with tones two or more octaves below CF. It was found that electrical stimulation of medial efferents can indeed inhibit ANF responses to tail-frequency tones. The amplitude of efferent inhibition depended on both sound level (largest near to threshold) and frequency (largest two to three octaves below CF). On average, inhibition of high-CF ANFs responding to 1 kHz tones was around 5 dB. Although an efferent reduction of basilar-membrane motion cannot be ruled out as the mechanism producing the inhibition of ANF responses to tail frequency tones, it seems more likely that efferents produce this effect by changing the micromechanics of the cochlear partition.

Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail

1. Discharges of neurons in the peripheral auditory system contain information about the temporal features of acoustic stimuli. Phase-locking of neurons in the anteroventral cochlear nucleus (AVCN) is usually reported to be less robust than in auditory nerve (AN) fibers, which provide their major input. In a companion paper we reported that some cells in AVCN of the cat show enhanced phase-locking compared with the AN when stimulated at the frequency to which they are most sensitive [characteristic frequency (CF)]. We called neurons "high-sync" when they showed vector strengths (R, a measure of phase-locking) > or = 0.9. Here we report phase-locking properties to stimuli at frequencies below CF. 2. Horseradish peroxidase-filled glass micropipettes or metal microelectrodes were inserted into the trapezoid body (TB), which is the large output tract of the AVCN. Acoustically driven fibers were classified on the basis of the shape of the poststimulus time (PST) histograms to short tone bursts at CF. We then presented low-frequency tones of increasing SPL and determined the maximum R value at 500 Hz (R500) for each fiber. Using the same experimental protocol we studied phase-locking in the ANs of two animals because maximal R values at the tuning curve tail have not been reported for AN fibers. 3. Although phase-locking in AN fibers is usually assumed to be independent of CF, we found that fibers with CF > 2 kHz tended to have higher R500 values than fibers with CF < or = 2 kHz. Moreover, R500 was > or = 0.9 in 20% (42 of 196) of the fibers studied and could be as high as 0.95. This population of fibers was defined as having "high-sync tails" and consisted almost entirely of fibers with low or medium spontaneous rate. 4. High-CF TB fibers stimulated at 500 Hz showed very high phase-locking. High-sync tails (R500 > or = 0.9) were found in 41 of 70 TB fibers. For a subset of these fibers (1/3 in total: 23 of 70) phase-locking was higher than is ever observed in the AN (R500 > or = 0.95); these fibers were defined as showing synchronization "enhancement." Virtually all fibers showing synchronization enhancement had primary-like-with-notch (PLN) PST histograms. Chopper and primary-like fibers showed high-sync tails for CFs > 3 kHz. 5. Synchronization filter functions were obtained for high-CF AN fibers by determining maximum synchronization for a range of stimuli below CF.(ABSTRACT TRUNCATED AT 400 WORDS)

Why is the 2f1−f2 distortion product maximum at f2/f1≊1.2?

It has been known for a long time that the acoustic distortion product 2f1−f2 measured in the ear canal is maximum when f2/f1≊1.2. It is now known that all the distortion products f2−n(f2−f1), for integer n, peak at the same frequency fmax(f2), that depends only on f2. Neural tuning curves frequently have a notched region where the tip meets the tail. The frequency of this notch is defined as fz(fCF). Here, fz depends on the characteristic frequency of the neuron fCF. Assuming that the distortion products are generated on the basilar membrane at the f2 place, fCF is associated with f2. When this is done, it is found experimentally (for the cat) that fz=fmax. In other words, it has been found experimentally that the maximum of the DP is at the same frequency as where the tuning curve tail and tip meet. This result implies that the micromechanics of the cochlea contains a mechanical circuit resonance at this frequency. This impedance must be connected across the inner hair cells, so that it ‘‘shorts out’’ the nerve excitation, reducing the IHC sensitivity at the resonance frequency, and inseries with the nonlinear generator, thereby maximally coupling the DP back into the cochlear fluid, and hence into the ear canal.

Psychoacoustical masking of one pure tone by another and its relation to a model of the mechanics of the basilar membrane

Accelerated psychoacoustical masking effects with level for simple tone maskers of higher frequency tones [Wegel and Lane, Phys. Rev. 23, 226–285 (1924); Duifhuis, J. Acoust. Soc. Am, 67, 914–927 (1980)] have clear correlates with nonlinear suppression and excitation phenomena in auditory nerve and basilar membrane responses [Abbas and Sachs, J. Acoust. Soc. Am. 59, 112–122 (1976); Patuzzi, Sellick, and Johnstone, Hear. Res. 13, 19–27 (1984); Robles et al., J. Acoust. Soc. Am. 80, 1364–1384 (1986)]. A signal processing model of basilar membrane response is presented that quantifies basilar membrane mechanics as two nonlinearly interacting filter responses: (i) a sensitive, narrow‐band compresslye response responsible for the tips of cochlear suppression and excitation tuning curves; and (ii) and insensitive, lowpass linearlike response responsible for the low‐frequency tails of tuning curves. Dual filter processing along with mutual suppression between the filters, described by the model, allows conceptualization of known psychoacoustics in terms of competing cochlear mechanical responses. Detailed model accounts of data and methods for estimating model parameters will be presented.

New insights in the evaluation of cochlear impairment.

A major new insight into cochlear mechanisms is the recognition of an active process, the cochlear amplifier, that contributes energy to the mechanical movement of the basilar membrane at low sound intensities. The extra energy makes possible the great sensitivity of hearing and also the very sharp tuning of individual neural units, ie, the tips of their tuning curves. The inner hair cells are the final receptor cells, but the outer hair cells are essential for the amplifier action. The amplifier is much more sensitive to anoxia, ototoxic drugs, noise, etc, than the inner hair cell system alone. Severe impairment of the amplifier causes a sensorineural hearing loss with recruitment. Only the tails of tuning curves remain. Thus the cochlea is a dual sensory system, a robust but insensitive broadly tuned passive component sided by a vulnerable, sensitive sharply tuned active component.

The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves in cats

Furosemide was injected intravenously in anesthetized cats while the endocochlear potential (EP) and tuning curves from fibers of the auditory nerve were simultaneously monitored in the same ear. The characteristic frequencies (CF's) of the fibers studied ranged from 0.25 to 28 kHz. Furosemide administration produced reversible, dose-related decreases in the EP which were accompanied by threshold elevations and alterations in the tuning curves of auditory nerve fibers. There was approximately l dB of threshold elevation for every millivolt decrease in the EP. For fibers with CF's above 3 kHz, threshold elevation at CF (in the tip of the tuning curve) was three times that in the tail of the tuning curve. Threshold elevation in the tip was always accompanied by threshold elevation in the tuning curve tail. Threshold elevation was dependent upon the CF of the fiber, with higher CF fibers showing larger threshold shifts than lower CF fibers. Threshold elevation was accompanied by a systematic shift in the CF of the fiber. Fibers with CF above 1 kHz exhibited downward shifts in CF, while those with CF less than 1 kHz generally exhibited upward shifts in CF.

Tails of tuning curves of auditory-nerve fibers.

Békésy's interest in improving telephone communication led him eventually to make observations on the mechanical properties of the basilar membrane. For apical parts of the membrane he obtained resonance curves with steep high-frequency slopes and gradual low-frequency slopes. Tuning curves for auditory-nerve fibers in anesthetized cats also show significant low-frequency tails. Even fibers with high characteristic frequencies (CF) respond to tones throughout a wide range of low and middle frequencies. For low-frequency tones at moderate and high stimulus levels the responses of high-CF fibers tend to be time-locked either to the same phase of the stimulus or to a phase that differs by a half cycle. For complex stimuli such as speech, which contains many low-frequency components, these fibers behave as broadly tuned elements, discharging with time patterns that are principally determined by the temporal characteristics of the acoustic waveform. Results of experiments using low- and high-frequency masking stimuli reinforce the view that responses of high-CF fibers to low-frequency stimuli should not be ignored in theories that seek to describe the role of the auditory nerve in speech communication.