Forward masking of the auditory nerve neurophonic (ANN) and the frequency following response (FFR)

doi:10.1016/0378-5955(85)90058-9

Hearing Research

Volume 20, Issue 1, 1985, Pages 45-62

https://doi.org/10.1016/0378-5955(85)90058-9 Get rights and content

Abstract

The forward masking behavior of two averaged neurophonic responses was examined in cats. The auditory nerve neurophonic (ANN) was recorded with bipolar electrodes placed on the auditory nerve as it exits the internal meatus. The frequency following response (FFR) was recorded using scalp electrodes placed at the vertex and below the stimulated ear. Masking functions (response amplitude vs masker level) for frequencies both above and below the probe frequency were recorded. From these masking functions, 30% iso-depression contours (forward masking tuning curves, FMTCs) were constructed. The time course of the recovery from forward masking was also examined.

It was found that the forward masking behavior of these neurophonics have many similarities to the behavior of other responses recorded using psychophysical and physiological methods. However, forward masking of the ANN and FFR has a number of unusual features. First, the best masking frequency (BMF), which in most forward masking studies is equal to the probe frequency, can be off-set from the probe frequency by as much as an octave. Second, the masker level at BMF can be as much as 30 dB below the probe level. Third, the magnitude of both of these off-sets is a function of the probe level. Fourth, low level neurophonic response could be enhanced by some forward ‘maskers’.

The features of neurophonic forward masking are discussed and a model of the neurophonics is suggested. This model is based on the spatial distribution of phase and amplitude in the phase-locked activity in the auditory nerve and it can qualitatively account for many of the properties of the neurophonics.

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The auditory nerve neurophonic (ANN) response is the mass potential correlate of phase-locked neural activity across AN fibers recorded near the cochlea, which can be dissociated from the cochlear microphonic (CM) response produced by hair cell activity (Fontenot et al., 2017; Snyder and Schreiner, 1984; Verschooten and Joris, 2014). The ANN shows properties that reflect neural coding not present in the CM, such as rectification and adaptation (e.g., Verschooten and Joris 2014), and these response properties are also present in the scalp FFR (Snyder and Schreiner, 1985). Damage to AN fiber terminals or a suppressed spike generation in the AN abolish both the ANN and the scalp FFR (Fontenot et al., 2017; Henry, 1995; Snyder and Schreiner, 1984).
Healthy aging may be associated with neural degeneration in the cochlea even before clinical hearing loss emerges. Reduction in frequency-following responses (FFRs) to tonal carriers in older clinically normal-hearing listeners has previously been reported, and has been argued to reflect an age-dependent decline in temporal processing in the central auditory system. Alternatively, age-dependent loss of auditory nerve fibers (ANFs) may have little effect on audiometric sensitivity and yet compromise the precision of neural phase-locking relying on joint activity across populations of fibers. This peripheral loss may, in turn, contribute to reduced neural synchrony in the brainstem as reflected in the FFR. Here, we combined human electrophysiology and auditory nerve (AN) modeling to investigate whether age-related changes in the FFR would be consistent with peripheral neural degeneration. FFRs elicited by pure tones and frequency sweeps at carrier frequencies between 200 and 1200 Hz were obtained in older (ages 48–76) and younger (ages 20–30) listeners, both groups having clinically normal audiometric thresholds up to 6 kHz. The same stimuli were presented to a computational model of the AN in which age-related loss of hair cells or ANFs was modelled using human histopathological data. In the older human listeners, the measured FFRs to both sweeps and pure tones were found to be reduced across the carrier frequencies examined. These FFR reductions were consistent with model simulations of age-related ANF loss. In model simulations, the phase-locked response produced by the population of remaining fibers decreased proportionally with increasing loss of the ANFs. Basal-turn loss of inner hair cells also reduced synchronous activity at lower frequencies, albeit to a lesser degree. Model simulations of age-related threshold elevation further indicated that outer hair cell dysfunction had no negative effect on phase-locked AN responses. These results are consistent with a peripheral source of the FFR reductions observed in older normal-hearing listeners, and indicate that FFRs at lower carrier frequencies may potentially be a sensitive marker of peripheral neural degeneration.
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For scalp-recorded neural synchronization (i.e., EFRs), the speech-like stimulus (described previously) was presented with a repetition rate of 3.1 Hz (leading to an interstimulus interval of 63 ms). Although the interstimulus interval is relatively short (63 ms), we did not expect spill-over effects from one stimulus presentation to the next as the timescale for recovery of forward masking at the auditory nerve, cochlear nucleus, superior olivary complex, and the inferior colliculus in rodents has been estimated to be within 30–50 ms (Gao and Berrebi, 2016; Ingham et al., 2016; Snyder and Schreiner, 1985; Verschooten et al., 2012). Furthermore, the interstimulus interval in previous investigations of the effects of age on EFRs in humans used only slightly longer intervals ranging from 80 to 100 ms (Anderson et al., 2012; Schoof and Rosen, 2016).
Hearing impairment in older people is thought to arise from impaired temporal processing in auditory circuits. We used a systems-level (scalp recordings) and a microcircuit-level (extracellular recordings) approach to investigate how aging affects the sensitivity to temporal envelopes of speech-like sounds in rats. Scalp-recorded potentials suggest an age-related increase in sensitivity to temporal regularity along the ascending auditory pathway. The underlying cellular changes in the midbrain were examined using extracellular recordings from inferior colliculus neurons. We observed an age-related increase in sensitivity to the sound's onset and temporal regularity (i.e., periodicity envelope) in the spiking output of inferior colliculus neurons, relative to their synaptic inputs (local field potentials). This relative enhancement for aged animals was most prominent for multi-unit (relative to single-unit) spiking activity. Spontaneous multi-unit, but not single-unit, activity was also enhanced in aged compared with young animals. Our results suggest that aging is associated with altered sensitivity to a sound's temporal regularities, and that these effects may be due to increased gain of neural network activity in the midbrain.
Auditory nerve neurophonic tuning curves produced by masking of round window responses
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In response to low-intensity, low-frequency, phase-locked tonal stimuli with non-alternating polarity, the time-averaged round window (RW) response of the gerbil is a mixture of the auditory nerve neurophonic (ANN) and cochlear microphonic (CM), with the former often being of equal or greater magnitude than the latter. Forward masking (using a conservative 25% amplitude reduction criterion) can be used to generate ANN tuning curves (TC). Most of these TCs are sharply tuned V-shaped functions. Harmonic distortion is often present in the ANN, especially in response to the lower-frequency (≤ 1 kz) or higher-intensity (? 50 dB) stimuli. The TCs created by forward masking of the harmonics are similar in appearance to those generated by masking the fundamental frequency of the ANN. When lower-frequency probe stimuli (≤ ≈ 1 kHz) are used, the frequency of the TC tip tends to be higher than that of the probe; with higher probe frequencies, the tip tends to be lower. Regardless of the frequency of the probe, the TC tip threshold occurs at an intensity level lower than that of the probe. The sharpness of these TCs generally increases as a function of the frequency of the probe stimulus and the values of Q_10dB are comparable to those of FTCs of cochlear nerve fibers of the gerbil. The amplitude of the ANN is often enhanced in response to a limited intensity range of forward maskers over a restricted range of frequencies that are outside the high-frequency boundary of the forward masker TC. By alternating the polarity of the probe stimulus, the CM can be canceled, allowing the effects of simultaneous maskers to be evaluated.
Tuning curves of the difference tone auditory nerve neurophonic
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When a pair of tonal stimuli of different frequencies (F₁ and F₂, where F₂ > F₁) are simultaneously presented to the ear, an electrical response with a frequency of F₂-F₁ can be recorded from the round window (RW) of the gerbil's cochlea. By using phase-locked tones of alternating polarity, the cochlear microphonics are canceled, leaving a time-averaged difference tone-auditory nerve neurophonic (DT-ANN). When the F, frequency ranges from 1.25 to 30 kHz and F₂−F₁ ≈ 900 Hz, a DT-ANN audiogram can be constructed which parallels (but is at least 10 dB more sensitive than) the compound action potential (CAP) audiogram. In addition to this DT response, a smaller magnitude, higher threshold response having a frequency of 2 DT can often be measured. Both the DT-ANN and the 2 DT-ANN show non-monotonic amplitude input-output functions. The DT- and 2 DT-ANN responses can be forward masked. Masking of low level (e.g., 30 dB SPL) probe stimuli results in DT- and 2 DT-ANN V-shaped tuning curves (TO with low tip thresholds (≈ 20–30 dB SPL) and a tip frequency close to that of F₁ and F₂. The Q_{10 dB} values of the forward masked DT-ANN TCs ranges from 1.54 to 20.0 for F₁ frequencies varying from 2 to 20 kHz, respectively. The V-shaped DT-ANN TCs generated with simultaneous maskers are often flanked, outside their high- and low-frequency slopes, by frequency-intensity domains where the masker enhances the amplitude of the DT-ANN response. These data (1) provide evidence that, in response to low-intensity tones, the DT-ANN is generated by a restricted population of neurons that have characteristic frequencies close to F₁ and F₂, and (2) provide evidence for sharply tuned, phase-locked activity occurring in response to low-intensity stimuli, by cochlear axons having characteristic frequencies as high as 20 kHz.
Auditory nerve neurophonic recorded from the round window of the Mongolian gerbil
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In the Mongolian gerbil, round window (RW) recordings of averaged responses to phase-locked acoustic stimuli which are not alternated in polarity can include both the cochlear microphonic (CM) and auditory nerve neurophonic (ANN). The ANN can dominate the recordings when the RW electrode is referenced to some portion of the body that allows the two electrodes to straddle the auditory nerve. Concentric bipolar RW electrodes are biased in favor of the CM. When there is a substantial ANN component in the RW response, as the sinusoidal stimulus intensity increases there is a non-monotonic increase of amplitude and a pronounced change of phase of the response. When the phase-locked stimuli are alternated in polarity in order to cancel the CM, a residual response is often observed. This residual response has twice the frequency of the stimulus and is decreased in amplitude by forward masking. It also shows a pattern of amplitude decrement following the stimulus onset, resembling adaptation of firing rate of cochlear nerve axons. Tetrodotoxin (TTX) eliminates the non-monotonic RW amplitude input-output (I/O) function, reduces the phase changes of the response as the stimulus intensity is increased, eliminates the residual non-canceled response to alternated stimuli, and the time-limited amplitude decrements which resemble adaptation. Following application of TTX, the RW response of the gerbil to stimuli with non-alternated polarity much more closely resembles the CM responses of other animals. It is concluded that the gerbil's residual response following cancellation of the CM is the ANN, and that the RW of the gerbil is a convenient site for recording measures of phase-locked cochlear axonal activity.
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Several strains of laboratory mouse (Mus musculus) have a pattern of hearing loss which resembles that found in humans. The C57BL/6 strain of mouse has a genetic defect that results in degeneration of the organ of Corti, originating in the basal, high-frequency region and then proceeding apically over time. The end result is a severe-to-profound sensorineural hearing loss (SNHL) by 14 months of age. In contrast, auditory function of the CBA strain remains normal through its early life span then slowly declines later in life, much like that typified by human presbycusis. The purpose of the present study was to compare ABR (peak 5) forward masking recovery functions in young, normal-hearing CBA and C57BL/6 mice to hearing-impaired C57BL/6 mice. ABR audiograms were obtained prior to collecting the tone-on-tone forward masking data. Masking was defined as a 50% reduction in the P5 component of the ABR, elicited and masked by 12 kHz tone bursts, using masker/probe time delays from 0 to 100 ms. Time constants were computed from an exponential model fit to the recovery functions (masker level vs. time delay). In hearing-impaired animals there was a significant increase in recovery from short-term adaptation as measured by the time constants, as well as a significant latency shift in the P5 component. The effects of SNHL on the recovery of the P5 component from short-term adaptation was comparable to that reported behaviorally for human hearing-impaired listeners and physiologically from the inferior colliculus (IC) of chinchillas suffering permanent threshold shifts.

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Forward masking of the auditory nerve neurophonic (ANN) and the frequency following response (FFR)

Abstract

Hearing Res.

Hearing Res.

Hearing Res.

Electroenceph. Clin. Neurophysiol.

Hearing Res.

Hearing Res.

Hearing Res.

Hearing Res.

Recovery from long-term and short-term adaptation of the whole nerve action potential

J. Acoust. Soc. Am.

AP responses in forward masking paradigms and their relationship to responses of auditory nerve fibers

J. Acoust. Soc. Am.

Two-tone suppression in auditory-nerve fibers: Extension of a stimulus-response relationship

J. Acoust. Soc. Am.

Synthetic whole nerve action potentials for the cat

J. Acoust. Soc. Am.

Physiological observations of auditory masking. I. Effects of masking duration

J. Neurophysiol.

Physiological observations of auditory masking. II. Effects of masking intensity

J. Neurophysiol.

Compound action potential (AP) tuning curves

J. Acoust. Soc. Am.

Cochlear mechanics, non-linearities and cochlear potentials

J. Acoust. Soc. Am.

Cochlear adaptation in guinea pigs: A quantitative description

Audiology

Simulation of cochlear action potentials recorded from the ear canal of man

The effects of high-pass noise on the scalp-recorded frequency following response (FFR) in humans and cats

J. Acoust. Soc. Am.

Synchrony of neural activity in electric responses evoked by transient acoustic stimuli

J. Acoust. Soc. Am.

Forward-masking AP tuning curves in normal and in acoustically traumatized ears

J. Acoust. Soc. Am.

AP measurements of short-term adaptation in normal and acoustically traumatized ears

J. Acoust. Soc. Am.