Clutter resilience via auditory stream segregation in echolocating greater mouse-eared bats.

Bats use echolocation to navigate and hunt in darkness, and must in that process segregate target echoes from unwanted clutter echoes. Bats may do this by approaching a target at steep angles relative to the plane of the background, utilizing their directional transmission and receiving systems to minimize clutter from background objects, but it remains unknown how bats negotiate clutter that cannot be spatially avoided. Here, we tested the hypothesis that when movement no longer offers spatial release, echolocating bats mitigate clutter by calling at lower source levels and longer call intervals to ease auditory streaming. We trained five greater mouse-eared bats (Myotis myotis) to land on a spherical loudspeaker with two microphones attached. We used a phantom-echo setup, where the loudspeaker/target transmitted phantom clutter echoes by playing back the bats' own calls at time delays of 1, 3 and 5 ms with a virtual target strength 7 dB higher than the physical target. We show that the bats successfully landed on the target, irrespective of the clutter echo delays. Rather than decreasing their source levels, the bats used similar source level distributions in clutter and control trials. Similarly, the bats did not increase their call intervals, but instead used the same distribution of call intervals across control and clutter trials. These observations reject our hypothesis, leading us to conclude that bats display great resilience to clutter via short auditory integration times and acute auditory stream segregation rather than via biosonar adjustments.

Monaural and dichotic forward masking in the dolphin's auditory system.

Short-latency auditory-evoked potentials (AEPs) were recorded non-invasively in the bottlenose dolphin Tursiops truncatus. The stimuli were two sound clicks that were played either monaurally (both clicks to one and the same acoustic window) or dichotically (the leading stimulus (masker) to one acoustic window and the delayed stimulus (test) to the other window). The ratio of the levels of the two stimuli was 0, 10, or 20 dB (at 10 and 20 dB, the leading stimulus was of a higher level). The inter-stimulus intervals (ISIs) varied from 0.15 to 10 ms. The test response magnitude was assessed by correlation analysis as a percentage of the control (non-masked) response. At monaural stimulation, the test response was of a constant magnitude (5-6% of the control) at ISIs of 0.15-0.3 ms and recovered at longer ISIs. At dichotic stimulation, the deepest suppression of the test response occurred at ISIs of 0.5-0.7 ms. The response was slightly suppressed at short ISIs (0.15-0.3 ms) and recovered at ISIs longer than 0.5-0.7 ms. The relation of parameters of the forward masking to echolocation in dolphins is discussed.

The influence of phoneme contexts on adaptation in vowel-evoked envelope following responses.

Repeated stimulus presentation leads to neural adaptation and consequent amplitude reduction in vowel-evoked envelope following responses (EFRs)-a response that reflects neural activity phase-locked to envelope periodicity. EFRs are elicited by vowels presented in isolation or in the context of other phonemes such as consonants in syllables. While context phonemes could exert some forward influence on vowel-evoked EFRs, they may reduce the degree of adaptation. Here, we evaluated whether the properties of context phonemes between consecutive vowel stimuli influence adaptation. EFRs were elicited by the low-frequency first formant (resolved harmonics) and middle-to-high-frequency second and higher formants (unresolved harmonics) of a male-spoken /i/ when the presence, number and predictability of context phonemes (/s/, /a/, /∫/ and /u/) between vowel repetitions varied. Monitored over four iterations of /i/, adaptation was evident only for EFRs elicited by the unresolved harmonics. EFRs elicited by the unresolved harmonics decreased in amplitude by ~16-20 nV (10%-17%) after the first presentation of /i/ and remained stable thereafter. EFR adaptation was reduced by the presence of a context phoneme, but the reduction did not change with their number or predictability. The presence of a context phoneme, however, attenuated EFRs by a degree similar to that caused by adaptation (~21-23 nV). Such a trade-off in the short- and long-term influence of context phonemes suggests that the benefit of interleaving EFR-eliciting vowels with other context phonemes depends on whether the use of consonant-vowel syllables is critical to improve the validity of EFR applications.

The rate of cochlear compression in a dolphin: a forward-masking evoked-potential study.

The "active" cochlear mechanism of hearing manifests in the cochlear compression. Investigations of compression in odontocetes help to determine the frequency limit of the active mechanism. The compression may be evaluated by comparison of low- and on-frequency masking. In a bottlenose dolphin, forward masking of auditory evoked potentials to tonal pips was investigated. Measurements were performed for test frequencies of 45 and 90 kHz. The low-frequency maskers were - 0.25 to - 0.75 oct relative the test. Masking efficiency was varied by masker-to-test delay variation from 2 to 20 ms, and masker levels at threshold (MLTs) were evaluated at each of the delays. It was assumed that low-frequency maskers were not subjected or little subjected to compression whereas on-frequency maskers were subjected equally to the test. Therefore, the compression rate was assessed as the slope of low-frequency MLT dependence on on-frequency MLT. For the 90-kHz test, the slopes were 0.63 and 0.18 dB/dB for masker of - 0.25 and - 0.5 oct, respectively. For the 45 kHz test, the slopes were 0.69 and 0.39 dB/dB for maskers of - 0.25 and - 0.5 oct. So, compression did not decay at the upper boundary of the hearing frequency range in the dolphin.

Nicotinic acetylcholine receptor subunit α7-knockout mice exhibit degraded auditory temporal processing.

The CHRNA7 gene that encodes the α7-subunit of the nicotinic acetylcholine receptor (α7-nAChR) has been associated with some autism spectrum disorders and other neurodevelopmental conditions characterized, in part, by auditory and language impairment. These conditions may include auditory processing disorders that represent impaired timing of neural activity, often accompanied by problems understanding speech. Here, we measure timing properties of sound-evoked activity via the auditory brainstem response (ABR) of α7-nAChR knockout mice of both sexes and wild-type colony controls. We find a significant timing delay in evoked ABR signals that represents midbrain activity in knockouts. We also examine spike-timing properties of neurons in the inferior colliculus, a midbrain nucleus that exhibits high levels of α7-nAChR during development. We find delays of evoked responses along with degraded spiking precision in knockout animals. We find similar timing deficits in responses of neurons in the superior paraolivary nucleus and ventral nucleus of the lateral lemniscus, which are brainstem nuclei thought to shape temporal precision in the midbrain. In addition, we find that other measures of temporal acuity including forward masking and gap detection are impaired for knockout animals. We conclude that altered temporal processing at the level of the brainstem in α7-nAChR-deficient mice may contribute to degraded spike timing in the midbrain, which may underlie the observed timing delay in the ABR signals. Our findings are consistent with a role for the α7-nAChR in types of neurodevelopmental and auditory processing disorders and we identify potential neural targets for intervention.NEW & NOTEWORTHY Disrupted signaling via the α7-nicotinic acetylcholine receptor (α7-nAChR) is associated with neurodevelopmental disorders that include impaired auditory processing. The underlying causes of dysfunction are not known but a common feature is abnormal timing of neural activity. We examined temporal processing of α7-nAChR knockout mice and wild-type controls. We found degraded spike timing of neurons in knockout animals, which manifests at the level of the auditory brainstem and midbrain.

Nonuniform impacts of forward suppression on neural responses to preferred stimuli and nonpreferred stimuli in the rat auditory cortex.

In natural conditions, human and animals need to extract target sound information from noisy acoustic environments for communication and survival. However, how the contextual environmental sounds impact the tuning of central auditory neurons to target sound source azimuth over a wide range of sound levels is not fully understood. Here, we determined the azimuth-level response areas (ALRAs) of rat auditory cortex neurons by recording their responses to probe tones varying with levels and sound source azimuths under both quiet (probe alone) and forward masking conditions (preceding noise + probe). In quiet, cortical neurons responded stronger to their preferred stimuli than to their nonpreferred stimuli. In forward masking conditions, an effective preceding noise reduced the extents of the ALRAs and suppressed the neural responses across the ALRAs by decreasing the response strength and lengthening the first-spike latency. The forward suppressive effect on neural response strength was increased with increasing masker level and decreased with prolonging the time interval between masker and probe. For a portion of cortical neurons studied, the effects of forward suppression on the response strength to preferred stimuli was weaker than those to nonpreferred stimuli, and the recovery from forward suppression of the response strength to preferred stimuli was earlier than that to nonpreferred stimuli. We suggest that this nonuniform forward suppression of neural responses to preferred stimuli and to nonpreferred stimuli is important for cortical neurons to maintain their relative stable preferences for target sound source azimuth and level in noisy acoustic environments.

Masking reduces orientation selectivity in rat visual cortex.

In visual masking the perception of a target stimulus is impaired by a preceding (forward) or succeeding (backward) mask stimulus. The illusion is of interest because it allows uncoupling of the physical stimulus, its neuronal representation, and its perception. To understand the neuronal correlates of masking, we examined how masks affected the neuronal responses to oriented target stimuli in the primary visual cortex (V1) of anesthetized rats (n = 37). Target stimuli were circular gratings with 12 orientations; mask stimuli were plaids created as a binarized sum of all possible target orientations. Spatially, masks were presented either overlapping or surrounding the target. Temporally, targets and masks were presented for 33 ms, but the stimulus onset asynchrony (SOA) of their relative appearance was varied. For the first time, we examine how spatially overlapping and center-surround masking affect orientation discriminability (rather than visibility) in V1. Regardless of the spatial or temporal arrangement of stimuli, the greatest reductions in firing rate and orientation selectivity occurred for the shortest SOAs. Interestingly, analyses conducted separately for transient and sustained target response components showed that changes in orientation selectivity do not always coincide with changes in firing rate. Given the near-instantaneous reductions observed in orientation selectivity even when target and mask do not spatially overlap, we suggest that monotonic visual masking is explained by a combination of neural integration and lateral inhibition.

Frequency Tuning of the Efferent Effect on Cochlear Gain in Humans.

Cochlear gain reduction via efferent feedback from the medial olivocochlear bundle is frequency specific (Guinan, Curr Opin Otolaryngol Head Neck Surg 18:447-453, 2010). The present study with humans used the Fixed Duration Masking Curve psychoacoustical method (Yasin et al., J Acoust Soc Am 133:4145-4155, 2013a; Yasin et al., Basic aspects of hearing: physiology and perception, pp 39-46, 2013b; Yasin et al., J Neurosci 34:15319-15326, 2014) to estimate the frequency specificity of the efferent effect at the cochlear level. The combined duration of the masker-plus-signal stimulus was 25 ms, within the efferent onset delay of about 31-43 ms (James et al., Clin Otolaryngol 27:106-112, 2002). Masker level (4.0 or 1.8 kHz) at threshold was obtained for a 4-kHz signal in the absence or presence of an ipsilateral 60 dB SPL, 160-ms precursor (200-Hz bandwidth) centred at frequencies between 2.5 and 5.5 kHz. Efferent-mediated cochlear gain reduction was greatest for precursors with frequencies the same as, or close to that of, the signal (gain was reduced by about 20 dB), and least for precursors with frequencies well removed from that of the signal (gain remained at around 40 dB). The tuning of the efferent effect filter (tuning extending 0.5-0.7 octaves above and below the signal frequency) is within the range obtained in humans using otoacoustic emissions (Lilaonitkul and Guinan, J Assoc Res Otolaryngol 10:459-470, 2009; Zhao and Dhar, J Neurophysiol 108:25-30, 2012). The 10 dB bandwidth of the efferent-effect filter at 4000 Hz was about 1300 Hz (Q(10) of 3.1). The FDMC method can be used to provide an unbiased measure of the bandwidth of the efferent effect filter using ipsilateral efferent stimulation.

Spatially extended forward suppression in primate auditory cortex.

When auditory neurons are stimulated with a pair of sounds, the preceding sound can inhibit the neural responses to the succeeding sound. This phenomenon, referred to as 'forward suppression', has been linked to perceptual forward masking. Previous studies investigating forward suppression typically measured the interaction between masker and probe sounds using a fixed sound location. However, in natural environments, interacting sounds often come from different spatial locations. The present study investigated two questions regarding forward suppression in the primary auditory cortex and adjacent caudal field of awake marmoset monkeys. First, what is the relationship between the location of a masker and its effectiveness in inhibiting neural response to a probe? Second, does varying the location of a masker change the spectral profile of forward suppression? We found that a masker can inhibit a neuron's response to a probe located at a preferred location even when the masker is located at a non-preferred location of a neuron. This is especially so for neurons in the caudal field. Furthermore, we found that the strongest forward suppression is observed when a masker's frequency is close to the best frequency of a neuron, regardless of the location of the masker. These results reveal, for the first time, the stability of forward masking in cortical processing of multiple sounds presented from different locations. They suggest that forward suppression in the auditory cortex is spectrally specific and spatially broad with respect to the frequency and location of the masker, respectively.

Estimation of Cochlear Frequency Selectivity Using a Convolution Model of Forward-Masked Compound Action Potentials.

PURPOSE: Frequency selectivity is a fundamental property of the peripheral auditory system; however, the invasiveness of auditory nerve (AN) experiments limits its study in the human ear. Compound action potentials (CAPs) associated with forward masking have been suggested as an alternative to assess cochlear frequency selectivity. Previous methods relied on an empirical comparison of AN and CAP tuning curves in animal models, arguably not taking full advantage of the information contained in forward-masked CAP waveforms. METHODS: To improve the estimation of cochlear frequency selectivity based on the CAP, we introduce a convolution model to fit forward-masked CAP waveforms. The model generates masking patterns that, when convolved with a unitary response, can predict the masking of the CAP waveform induced by Gaussian noise maskers. Model parameters, including those characterizing frequency selectivity, are fine-tuned by minimizing waveform prediction errors across numerous masking conditions, yielding robust estimates. RESULTS: The method was applied to click-evoked CAPs at the round window of anesthetized chinchillas using notched-noise maskers with various notch widths and attenuations. The estimated quality factor Q10 as a function of center frequency is shown to closely match the average quality factor obtained from AN fiber tuning curves, without the need for an empirical correction factor. CONCLUSION: This study establishes a moderately invasive method for estimating cochlear frequency selectivity with potential applicability to other animal species or humans. Beyond the estimation of frequency selectivity, the proposed model proved to be remarkably accurate in fitting forward-masked CAP responses and could be extended to study more complex aspects of cochlear signal processing (e.g., compressive nonlinearities).