Jörg Lewald

High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication

SummaryTransmission and reception of high-frequency sound in the natural environment of bushcrickets (Tettigonia viridissima L.) was studied using the activity of an identified neuron in the insects auditory pathway as a “biological microphone”. Different positions of the receiver within the habitat were simulated by systematic variation of the distance from a loudspeaker and the height above the ground. Attenuation and filtering properties of the habitat were investigated with pure-tone frequencies between 5 and 40 kHz. Sound attenuation in excess of the attenuation due to geometrical spreading alone increased with increasing frequency, distance between sender and receiver, and decreasing height within the vegetation (Figs. 2–4). The data also confirm the existence of two kinds of excess attenuation. The amount of amplitude fluctuations in the sound signals was investigated by analysing the variability of the neuronal responses at a given receiver position. Variability increased with decreasing bandwidth of a noise signal at some distance from the loadspeaker. The variability in the responses to pure tones increased with both increasing frequency and distance from the source (Fig. 7). In the selected habitat, the temporal pattern of the natural calling song of male T. viridissima was very reliably reflected in the activity of the recorded neuron up to a distance of 30 m at the top of the vegetation, and 15–20 m near ground level (Figs. 5, 8). The maximum hearing distance in response to the calling song was about 40 m. Environmental constraints on long-range acoustic communication in the habitat are discussed in relation to possible adaptations of both the signal structure and the behavior of the insects.

Vertical sound localization in blind humans

It is widely held that early-blind people compensate their visual loss by a general sharpening of spatial hearing. The present study reports a possible exception to this view: when the vertical position (elevation) of a sound source had to be localized, four out of six early-blind subjects exhibited systematic deviations in pointing, while two early-blind subjects were as accurate as sighted controls. On the other hand, blind and sighted individuals were able to judge relative positions of different sound locations with similar precision. These results suggest that visual experience may be used to accurately calibrate the relation between the vertical coordinates of auditory space and body, but is not needed to develop sufficiently high resolution of spatial hearing.

Sound localization with eccentric head position

This study investigates the influence of head-to-trunk position on auditory localization in humans. Various methods of head pointing, of two-alternative forced choice, and hand pointing were employed. Head-pointing toward actual sound sources in darkness, by using only the subjective median plane of the head as a reference, resulted in systematic underestimations of target eccentricity. The deviations of the terminal head position from the target shifted with a mean slope of approximately 0.1 degrees per degree change in head position. A corresponding shift in the localization of virtual sound sources (presented via headphones during eccentric head positions) was demonstrated by requiring forced-choice (left or right) responses with respect to the subjective median plane of the head. Head pointing toward remembered auditory targets in darkness resulted in undershoots similar to those found with actual targets. However, when a visual marker of the actual median plane of the head was additionally presented to the subject during these tasks (by a laser attached to the head that projected a spot onto a screen), sound localization was fairly accurate. Localization of eccentric auditory targets by using a swivel hand pointer also showed systematic errors similar to those found with head pointing in darkness when the head was simultaneously oriented toward the sound. When the head remained in alignment with the trunk, hand pointing resulted in overshooting responses. These results may be related to neural processes, presumably in the posterior parietal cortex, that transform auditory and visual spatial coordinates into a common, trunk-centered, frame of reference.

The effect of gaze eccentricity on perceived sound direction and its relation to visual localization

This study investigates the influence of eye position on the localization of a free-field sound source by employing a pointing method. While fixating visual targets in various directions, the subjects indicated the perceived direction of a sound source by adjusting the azimuthal angle of a swivel pointer. The perceived sound azimuth shifted consistently opposite to the direction of eccentric gaze. i.e. to the left when gaze was to the right and vice versa. This shift resembled an approximately linear function of horizontal gaze direction. The mean magnitude of the shift was 3.1 degrees when the gaze was 45 degrees to the side (mean slope 0.069 degrees per degree eccentricity in gaze direction). An additional experiment investigated the relation of this effect to visual localization. Using the same method, the shift of perceived visual azimuth was measured as a function of gaze direction. The results indicate a shift in the same direction as the auditory shift (opposite to the direction of eccentric gaze), but with a significantly greater magnitude, which was 5.7 degrees for 45 degrees eccentricity in gaze direction. The perceived shifts of sound direction depending on gaze eccentricity may result from incomplete transformations of the auditory spatial coordinates from a craniocentric to an oculocentric frame of reference within neural maps of space, as has been suggested by previous neurophysiological investigations.

Eye-position effects in directional hearing.

The influence of gaze direction on azimuthal sound localization was investigated by presenting free-field acoustical stimuli in combination with a visual fixation task. In Experiment 1, a two-alternative forced-choice method was employed. While fixating visual targets, subjects judged whether noise bursts, presented from various directions, were perceived as being on the left or right of either a visual reference indicating straight ahead or the subjective straight-ahead direction. The psychometric functions measured with the first task shifted consistently opposite to the direction of eccentric gaze, i.e., the location of the auditory stimulus was perceived as shifted toward the direction of gaze. The mean magnitude of the shift was 4.7 degrees over a range of fixation angles up to 45 degrees on either side. Without an external reference indicating straight ahead, shifts of sound localization were inconsistent, either opposite or toward the direction of fixation in individual subjects. In Experiment 2, subjects orientated their head toward sound stimuli while fixating visual targets in various directions. As in Experiment 1, head position as a measure of sound localization shifted significantly toward the direction of eccentric gaze when a visual reference of the head median plane was present, and the results were inconsistent across subjects when it was absent. The results indicate a significant effect of gaze direction on the spatial agreement of auditory and visual perception which may be based on the superposition of distinct auditory and visual eye-position effects. The effect is in agreement with previous neurophysiological results that have suggested an incomplete neural transformation of auditory spatial coordinates from a craniocentric into an oculocentric frame of reference.

Auditory-visual spatial integration: A new psychophysical approach using laser pointing to acoustic targets

The alignment of auditory and visual spatial perception was investigated in four experiments, employing a method of laser pointing toward acoustic targets in combination with various tasks of visual fixation in six subjects. Subjects had to fixate either a target LED or a laser spot projected on a screen in a dark, anechoic room and, while doing so, direct the laser beam toward the perceived azimuthal position of the sound stimulus (bandpass-filtered noise; bandwidth 1-3 kHz; 70 dB sound pressure level, duration 10 s). The sound was produced by one of nine loudspeakers, located behind the acoustically transparent screen between 22 degrees to the left and 22 degrees to the right of straight ahead. Systematic divergences between sound azimuth and laser adjustment were found, depending on the instructions given to the subjects. The eccentricity of acoustic targets was generally overestimated by up to 10.4 degrees with an only slight influence of gaze direction on this effect. When the sound source was straight ahead, gaze direction had a substantial influence in that the laser adjustments deviated by up to 5.6 degrees from sound azimuth, toward the side to which the gaze was directed. This effect of eye position decreased with increasing eccentricity of the sound. These results can be explained by the interactive effects of four distinct factors: the lateral overestimation of the auditory eccentricity, the effect of eye position on sound localization, the effect of the retinal eccentricity on visual localization, and the extraretinal effect of eye position on visual localization.

Visual and proprioceptive shifts in perceived egocentric direction induced by eye-position.

The relation of three main effects of eye-position on perceived direction was investigated using a method of hand pointing in the horizontal plane: (1) Retinal eccentricity is overestimated with respect to the fovea by a constant factor of 2.6 degrees; (2) an extraretinal signal induces a shift in perceived visual direction (slope 0.12) that is opposite to the direction of eccentric gaze; and (3) the perceived position of the median plane of the head shifts toward the direction of eccentric eye-position (slope 0.23) while perceived trunk position remains unchanged.

Opposing effects of head position on sound localization in blind and sighted human subjects

Up to now, there is an unsolved contradiction between the view that the development of an auditory spatial representation needs calibration by vision and the psychophysical demonstration of quite precise sound localization in early blind humans. The present study provides a link between these two competing conceptions. Two experiments were conducted with congenitally or early blind subjects and sighted controls. In the first experiment, subjects pointed with their head to actual sound sources located in the azimuthal plane. In the second experiment, lateralization of dichotic sound stimuli, presented via headphones, was investigated with variation of head‐to‐trunk position. The results showed opposing systematic errors of sound localization or lateralization, depending on head position, made by blind and sighted subjects. These differences suggest that audiomotor feedback replaces vision so as to calibrate auditory space in blind individuals. That is, in contrast to the widespread opinion of compensation of visual loss by a general sharpening of audition, compensatory plasticity in the blind may specifically be related to enhanced processing of proprioceptive and vestibular information with the auditory spatial input.

Influence of head-to-trunk position on sound lateralization

Abstract The effect of horizontal head position on the lateralization of dichotic sound stimuli was investigated in four experiments. In experiment 1, subjects adjusted the interaural level difference (ILD) of a stimulus (band-pass noise) to the subjective auditory median plane (SAMP) while simultaneously directing the beam of a laser attached to the head to visual targets in various directions. The adjustments were significantly correlated with head position, shifting in a direction toward the side to which the head was turned. This result was replicated in experiment 2, which employed a two-alternative forced-choice method, in which stimuli of different ILD were presented and left/right judgments were made. In both experiments, the average magnitude of the shift of the SAMP was about 1 dB over the range of head positions from straight ahead to 60° to the side. The shift of the SAMP indicates that any shift in head position induces a change in sound lateralization in the opposite direction, i.e., the intracranial sound image is shifted slightly to the left when the head is directed to the right and to the right when the head is to the left. In experiments 3 and 4, the effect of head position was compared with that of eye position by using the same methods as in experiment 2. Both shifts in SAMP, induced by either head- or eye-position changes, are in the same direction and, on average, of about the same magnitude (experiment 3), and head- and eye-position effects compensate approximately for each other during variations of head position when the gaze remains fixed to a visual target in space (experiment 4).

More accurate sound localization induced by short-term light deprivation.

Crossmodal reorganization processes in the brain are mainly associated with early blindness, on the assumption that recruitment of genuine visual areas, such as primary visual cortex, for non-visual functions results in superior auditory and tactile performance of blind, compared to sighted, humans. This study shows that in sighted subjects the accuracy of sound localization, measured by a task of head pointing to acoustic targets, is reversibly increased after short-term light deprivation of 90 min. However, only the systematic deviations from target positions (constant error) were reduced after light deprivation, while the general precision of head pointing remained unchanged. Return to pre-deprivation values was observed after 180 min of re-exposure to light. The post-deprivation change was similar, though less in magnitude, to the effect of blindness that was demonstrated previously. Generally, these findings indicate that auditory-visual crossmodal plasticity can be quite rapidly initiated by deprivation of the visual cortex from visual input. It seems possible that visual deprivation has an influence on neuronal circuits, that are involved in processing of auditory information in visual brain areas of normal sighted humans. Since exclusively the constant error in sound localization, not general performance, was changed, the present effect of visual deprivation may, however, not be attributable to reorganization processes in the sense of a compensation for the absence of vision. It is more likely that the observed change in accuracy was specifically induced by the absence of visual calibration of the neural representation of auditory space during light deprivation.