Psychophysical evidence for auditory motion parallax.

Distance is important: From an ecological perspective, knowledge about the distance to either prey or predator is vital. However, the distance of an unknown sound source is particularly difficult to assess, especially in anechoic environments. In vision, changes in perspective resulting from observer motion produce a reliable, consistent, and unambiguous impression of depth known as motion parallax. Here we demonstrate with formal psychophysics that humans can exploit auditory motion parallax, i.e., the change in the dynamic binaural cues elicited by self-motion, to assess the relative depths of two sound sources. Our data show that sensitivity to relative depth is best when subjects move actively; performance deteriorates when subjects are moved by a motion platform or when the sound sources themselves move. This is true even though the dynamic binaural cues elicited by these three types of motion are identical. Our data demonstrate a perceptual strategy to segregate intermittent sound sources in depth and highlight the tight interaction between self-motion and binaural processing that allows assessment of the spatial layout of complex acoustic scenes.

Modulation of auditory percepts by transcutaneous electrical stimulation.

Transcutaneous, electrical stimulation with electrodes placed on the mastoid processes represents a specific way to elicit vestibular reflexes in humans without active or passive subject movements, for which the term galvanic vestibular stimulation was coined. It has been suggested that galvanic vestibular stimulation mainly affects the vestibular periphery, but whether vestibular hair cells, vestibular afferents, or a combination of both are excited, is still a matter of debate. Galvanic vestibular stimulation has been in use since the late 18th century, but despite the long-known and well-documented effects on the vestibular system, reports of the effect of electrical stimulation on the adjacent cochlea or the ascending auditory pathway are surprisingly sparse. The present study examines the effect of transcutaneous, electrical stimulation of the human auditory periphery employing evoked and spontaneous otoacoustic emissions and several psychoacoustic measures. In particular, level growth functions of distortion product otoacoustic emissions were recorded during electrical stimulation with alternating currents (2 Hz, 1-4 mA in 1 mA-steps). In addition, the level and frequency of spontaneous otoacoustic emissions were followed before, during, and after electrical stimulation (2 Hz, 1-4 mA). To explore the effect of electrical stimulation on the retrocochlear level (i.e. on the ascending auditory pathway beyond the cochlea), psychoacoustic experiments were carried out. Specifically, participants indicated whether electrical stimulation (4 Hz, 2 and 3 mA) induced amplitude modulations of the perception of a pure tone, and of auditory illusions after presentation of either an intense, low-frequency sound (Bounce tinnitus) or a faint band-stop noise (Zwicker tone). These three psychoacoustic measures revealed significant perceived amplitude modulations during electrical stimulation in the majority of participants. However, no significant changes of evoked and spontaneous otoacoustic emissions could be detected during electrical stimulation relative to recordings without electrical stimulation. The present findings show that cochlear function, as assessed with spontaneous and evoked otoacoustic emissions, is not affected by transcutaneous electrical stimulation, at the currents used in this study. Psychoacoustic measures like pure tone perception, but also auditory illusions, are affected by electrical stimulation. This indicates that activity of the retrocochlear ascending auditory pathway is modulated during transcutaneous electrical stimulation.

Human Exploration of Enclosed Spaces through Echolocation.

Some blind humans have developed echolocation, as a method of navigation in space. Echolocation is a truly active sense because subjects analyze echoes of dedicated, self-generated sounds to assess space around them. Using a special virtual space technique, we assess how humans perceive enclosed spaces through echolocation, thereby revealing the interplay between sensory and vocal-motor neural activity while humans perform this task. Sighted subjects were trained to detect small changes in virtual-room size analyzing real-time generated echoes of their vocalizations. Individual differences in performance were related to the type and number of vocalizations produced. We then asked subjects to estimate virtual-room size with either active or passive sounds while measuring their brain activity with fMRI. Subjects were better at estimating room size when actively vocalizing. This was reflected in the hemodynamic activity of vocal-motor cortices, even after individual motor and sensory components were removed. Activity in these areas also varied with perceived room size, although the vocal-motor output was unchanged. In addition, thalamic and auditory-midbrain activity was correlated with perceived room size; a likely result of top-down auditory pathways for human echolocation, comparable with those described in echolocating bats. Our data provide evidence that human echolocation is supported by active sensing, both behaviorally and in terms of brain activity. The neural sensory-motor coupling complements the fundamental acoustic motor-sensory coupling via the environment in echolocation.SIGNIFICANCE STATEMENT Passive listening is the predominant method for examining brain activity during echolocation, the auditory analysis of self-generated sounds. We show that sighted humans perform better when they actively vocalize than during passive listening. Correspondingly, vocal motor and cerebellar activity is greater during active echolocation than vocalization alone. Motor and subcortical auditory brain activity covaries with the auditory percept, although motor output is unchanged. Our results reveal behaviorally relevant neural sensory-motor coupling during echolocation.

Dependence of auditory spatial updating on vestibular, proprioceptive, and efference copy signals.

Humans localize sounds by comparing inputs across the two ears, resulting in a head-centered representation of sound-source position. When the head moves, information about head movement must be combined with the head-centered estimate to correctly update the world-centered sound-source position. Spatial updating has been extensively studied in the visual system, but less is known about how head movement signals interact with binaural information during auditory spatial updating. In the current experiments, listeners compared the world-centered azimuthal position of two sound sources presented before and after a head rotation that depended on condition. In the active condition, subjects rotated their head by ∼35° to the left or right, following a pretrained trajectory. In the passive condition, subjects were rotated along the same trajectory in a rotating chair. In the cancellation condition, subjects rotated their head as in the active condition, but the chair was counter-rotated on the basis of head-tracking data such that the head effectively remained fixed in space while the body rotated beneath it. Subjects updated most accurately in the passive condition but erred in the active and cancellation conditions. Performance is interpreted as reflecting the accuracy of perceived head rotation across conditions, which is modeled as a linear combination of proprioceptive/efference copy signals and vestibular signals. Resulting weights suggest that auditory updating is dominated by vestibular signals but with significant contributions from proprioception/efference copy. Overall, results shed light on the interplay of sensory and motor signals that determine the accuracy of auditory spatial updating.

Amplitude-modulation detection by gerbils in reverberant sound fields.

Reverberation can dramatically reduce the depth of amplitude modulations which are critical for speech intelligibility. Psychophysical experiments indicate that humans' sensitivity to amplitude modulation in reverberation is better than predicted from the acoustic modulation depth at the receiver position. Electrophysiological studies on reverberation in rabbits highlight the contribution of neurons sensitive to interaural correlation. Here, we use a prepulse-inhibition paradigm to quantify the gerbils' amplitude modulation threshold in both anechoic and reverberant virtual environments. Data show that prepulse inhibition provides a reliable method for determining the gerbils' AM sensitivity. However, we find no evidence for perceptual restoration of amplitude modulation in reverberation. Instead, the deterioration of AM sensitivity in reverberant conditions can be quantitatively explained by the reduced modulation depth at the receiver position. We suggest that the lack of perceptual restoration is related to physical properties of the gerbil's ear input signals and inner-ear processing as opposed to shortcomings of their binaural neural processing.

Discovering your inner bat: echo-acoustic target ranging in humans.

Echolocation is typically associated with bats and toothed whales. To date, only few studies have investigated echolocation in humans. Moreover, these experiments were conducted with real objects in real rooms; a configuration in which features of both vocal emissions and perceptual cues are difficult to analyse and control. We investigated human sonar target-ranging in virtual echo-acoustic space, using a short-latency, real-time convolution engine. Subjects produced tongue clicks, which were picked up by a headset microphone, digitally delayed, convolved with individual head-related transfer functions and played back through earphones, thus simulating a reflecting surface at a specific range in front of the subject. In an adaptive 2-AFC paradigm, we measured the perceptual sensitivity to changes of the range for reference ranges of 1.7, 3.4 or 6.8 m. In a follow-up experiment, a second simulated surface at a lateral position and a fixed range was added, expected to act either as an interfering masker or a useful reference. The psychophysical data show that the subjects were well capable to discriminate differences in the range of a frontal reflector. The range-discrimination thresholds were typically below 1 m and, for a reference range of 1.7 m, they were typically below 0.5 m. Performance improved when a second reflector was introduced at a lateral angle of 45°. A detailed analysis of the tongue clicks showed that the subjects typically produced short, broadband palatal clicks with durations between 3 and 15 ms, and sound levels between 60 and 108 dB. Typically, the tongue clicks had relatively high peak frequencies around 6 to 8 kHz. Through the combination of highly controlled psychophysical experiments in virtual space and a detailed analysis of both the subjects' performance and their emitted tongue clicks, the current experiments provide insights into both vocal motor and sensory processes recruited by humans that aim to explore their environment by echolocation.

The sonar aperture and its neural representation in bats.

As opposed to visual imaging, biosonar imaging of spatial object properties represents a challenge for the auditory system because its sensory epithelium is not arranged along space axes. For echolocating bats, object width is encoded by the amplitude of its echo (echo intensity) but also by the naturally covarying spread of angles of incidence from which the echoes impinge on the bat's ears (sonar aperture). It is unclear whether bats use the echo intensity and/or the sonar aperture to estimate an object's width. We addressed this question in a combined psychophysical and electrophysiological approach. In three virtual-object playback experiments, bats of the species Phyllostomus discolor had to discriminate simple reflections of their own echolocation calls differing in echo intensity, sonar aperture, or both. Discrimination performance for objects with physically correct covariation of sonar aperture and echo intensity ("object width") did not differ from discrimination performances when only the sonar aperture was varied. Thus, the bats were able to detect changes in object width in the absence of intensity cues. The psychophysical results are reflected in the responses of a population of units in the auditory midbrain and cortex that responded strongest to echoes from objects with a specific sonar aperture, regardless of variations in echo intensity. Neurometric functions obtained from cortical units encoding the sonar aperture are sufficient to explain the behavioral performance of the bats. These current data show that the sonar aperture is a behaviorally relevant and reliably encoded cue for object size in bat sonar.

Localization dominance and the effect of frequency in the Mongolian Gerbil, Meriones unguiculatus.

Due to its good low-frequency hearing, the Mongolian Gerbil (Meriones unguiculatus) has become a well-established animal model for human hearing. In humans, sound localization in reverberant environments is facilitated by the precedence effect, i.e., the perceptual suppression of spatial information carried by echoes. The current study addresses the question whether gerbils are a valid animal model for such complex spatial processing. Specifically, we quantify localization dominance, i.e., the fact that in the context of precedence, only the directional information of the sound which reaches the ear first dominates the perceived position of a sound source whereas directional information of the delayed echoes is suppressed. As localization dominance is known to be stimulus-dependent, we quantified the extent to which the spectral content of transient sounds affects localization dominance in the gerbil. The results reveal that gerbils show stable localization dominance across echo delays, well comparable to humans. Moreover, localization dominance systematically decreased with increasing center frequency, which has not been demonstrated in an animal before. These findings are consistent with an important contribution of peripheral-auditory processing to perceptual localization dominance. The data show that the gerbil is an excellent model to study the neural basis of complex spatial-auditory processing.

Psychophysical and physiological evidence for fast binaural processing.

The mammalian auditory system is the temporally most precise sensory modality: To localize low-frequency sounds in space, the binaural system can resolve time differences between the ears with microsecond precision. In contrast, the binaural system appears sluggish in tracking changing interaural time differences as they arise from a low-frequency sound source moving along the horizontal plane. For a combined psychophysical and electrophysiological approach, we created a binaural stimulus, called "Phasewarp," that can transmit rapid changes in interaural timing. Using this stimulus, the binaural performance in humans is significantly better than reported previously and comparable with the monaural performance revealed with amplitude-modulated stimuli. Parallel, electrophysiological recordings of binaural brainstem neurons in the gerbil show fast temporal processing of monaural and different types of binaural modulations. In a refined electrophysiological approach that was matched to the psychophysics, the seemingly faster binaural processing of the Phasewarp was confirmed. The current data provide both psychophysical and physiological evidence against a general, hard-wired binaural sluggishness and reconcile previous contradictions of electrophysiological and psychophysical estimates of temporal binaural performance.

Psychophysical and neurophysiological hearing thresholds in the bat Phyllostomus discolor.

Absolute hearing thresholds in the spear-nosed bat Phyllostomus discolor have been determined both with psychophysical and neurophysiological methods. Neurophysiological data have been obtained from two different structures of the ascending auditory pathway, the inferior colliculus and the auditory cortex. Minimum auditory thresholds of neurons are very similar in both structures. Lowest absolute thresholds of 0 dB SPL are reached at frequencies from about 35 to 55 kHz in both cases. Overall behavioural sensitivity is roughly 20 dB better than neural sensitivity. The behavioural audiogram shows a first threshold dip around 23 kHz but threshold was lowest at 80 kHz (-10 dB SPL). This high sensitivity at 80 kHz is not reflected in the neural data. The data suggest that P. discolor has considerably better absolute auditory thresholds than estimated previously. The psychophysical and neurophysiological data are compared to other phyllostomid bats and differences are discussed.

Perceptual interaction between carrier periodicity and amplitude-modulation in the gerbil (Meriones unguiculatus).

Due to its extended low-frequency hearing, the Mongolian gerbil (Meriones unguiculatus) has become a well-established animal model for human auditory processing. Here, two experiments are presented which quantify the gerbil's sensitivity to amplitude modulation (AM) and carrier periodicity (CP) in broad-band stimuli. Two additional experiments investigate a possible interaction of the two types of periodicity. The results show that overall sensitivity to AM and CP is considerably less than in humans (by at least 10 dB). The gerbil's amplitude-modulation sensitivity is almost independent of modulation frequency up to a modulation frequency of 1 kHz. Above, amplitude-modulation sensitivity deteriorates dramatically. On the basis of individual animals, carrier-periodicity detection may improve with increasing fundamental frequency up to about 500 Hz or may be independent of fundamental frequency. Amplitude-modulation thresholds are consistent with the hypothesis that intensity difference limens in the gerbil may be considerably worse than in humans, leading to the relative insensitivity for low modulation frequencies. Unlike in humans, inner-ear filtering appears not to limit amplitude-modulation sensitivity in the gerbil. Carrier-periodicity sensitivity changes with fundamental frequency similar to humans. Unlike in humans, there is no systematic interaction between AM and CP in the gerbil. This points to a relatively independent processing of the perceptual cues associated with AM and CP.

A neural correlate of stochastic echo imaging.

Bats quickly navigate through a highly structured environment relying on echolocation. Large natural objects in the environment, like bushes or trees, produce complex stochastic echoes, which can be characterized by the echo roughness. Previous work has shown that bats can use echo roughness to classify the stochastic properties of natural objects. This study provides both psychophysical and electrophysiological data to identify a neural correlate of statistical echo analysis in the bat Phyllostomus discolor. Psychophysical results show that the bats require a fixed minimum roughness of 2.5 (in units of base 10 logarithm of the stimulus fourth moment) for roughness discrimination. Electrophysiological results reveal a subpopulation of 15 of 94 recorded cortical units, located in an anterior region of auditory cortex, whose rate responses changed significantly with echo roughness. It is shown that the behavioral ability to discriminate differences in the statistics of complex echoes can be quantitatively predicted by the neural responses of this subpopulation of auditory-cortical neurons.