Sound localization by barn owls in a simulated echoic environment

We examined the accuracy and precision with which the barn owl (Tyto alba) turns its head toward sound sources under conditions that evoke the precedence effect (PE) in humans. Stimuli consisted of 25-ms noise bursts emitted from two sources, separated horizontally by 40 degrees, and temporally by 3-50 ms. At delays from 3 to 10 ms, head turns were always directed at the leading source, and were nearly as accurate and precise as turns toward single sources, indicating that the leading source dominates perception. This lead dominance is particularly remarkable, first, because on some trials, the lagging source was significantly higher in amplitude than the lead, arising from the directionality of the owl's ears, and second, because the temporal overlap of the two sounds can degrade the binaural cues with which the owl localizes sounds. With increasing delays, the influence of the lagging source became apparent as the head saccades became increasingly biased toward the lagging source. Furthermore, on some of the trials at delays > or = 20 ms, the owl turned its head, first, in the direction of one source, and then the other, suggesting that it was able to resolve two separately localizable sources. At all delays <50 ms, response latencies were longer for paired sources than for single sources. With the possible exception of response latency, these findings demonstrate that the owl exhibits precedence phenomena in sound localization similar to those in humans and cats, and provide a basis for comparison with neurophysiological data.     

Neural correlates of the precedence effect in the inferior colliculus of behaving cats

Several auditory spatial illusions, collectively called the precedence effect (PE), occur when transient sounds are presented from two different spatial locations but separated in time by an interstimulus delay (ISD). For ISDs in the range of localization dominance (<10 ms), a single fused sound is typically located near the leading source location only, as if the location of the lagging source were suppressed. For longer ISDs, both the leading and lagging sources can be heard and localized, and the shortest ISD where this occurs is called the echo threshold. Previous physiological studies of the extracellular responses of single neurons in the inferior colliculus (IC) of anesthetized cats and unanesthetized rabbits with sounds known to elicit the PE have shown correlates of these phenomena though there were differences in the physiologically measured echo thresholds. Here we recorded in the IC of awake, behaving cats using stimuli that we have shown to evoke behavioral responses that are consistent with the precedence effect. For small ISDs, responses to the lag were reduced or eliminated consistent with psychophysical data showing that sound localization is based on the leading source. At longer ISDs, the responses to the lagging source recovered at ISDs comparable to psychophysically measured echo thresholds. Thus it appears that anesthesia, and not species differences, accounts for the discrepancies in the earlier studies.     

Sensitivity of auditory cortical neurons to the locations of leading and lagging sounds

We recorded unit activity in the auditory cortex (fields A1, A2, and PAF) of anesthetized cats while presenting paired clicks with variable locations and interstimulus delays (ISDs). In human listeners, such sounds elicit the precedence effect, in which localization of the lagging sound is impaired at ISDs less, similar10 ms. In the present study, neurons typically responded to the leading stimulus with a brief burst of spikes, followed by suppression lasting 100-200 ms. At an ISD of 20 ms, at which listeners report a distinct lagging sound, only 12% of units showed discrete lagging responses. Long-lasting suppression was found in all sampled cortical fields, for all leading and lagging locations, and at all sound levels. Recordings from awake cats confirmed this long-lasting suppression in the absence of anesthesia, although recovery from suppression was faster in the awake state. Despite the lack of discrete lagging responses at delays of 1-20 ms, the spike patterns of 40% of units varied systematically with ISD, suggesting that many neurons represent lagging sounds implicitly in their temporal firing patterns rather than explicitly in discrete responses. We estimated the amount of location-related information transmitted by spike patterns at delays of 1-16 ms under conditions in which we varied only the leading location or only the lagging location. Consistent with human psychophysical results, transmission of information about the leading location was high at all ISDs. Unlike listeners, however, transmission of information about the lagging location remained low, even at ISDs of 12-16 ms.     

Responses of auditory cortical neurons to pairs of sounds: correlates of fusion and localization

When two brief sounds arrive at a listener's ears nearly simultaneously from different directions, localization of the sounds is described by "the precedence effect." At inter-stimulus delays (ISDs) <5 ms, listeners typically report hearing not two sounds but a single fused sound. The reported location of the fused image depends on the ISD. At ISDs of 1-4 ms, listeners point near the leading source (localization dominance). As the ISD is decreased from 0.8 to 0 ms, the fused image shifts toward a location midway between the two sources (summing localization). When an inter-stimulus level difference (ISLD) is imposed, judgements shift toward the more intense source. Spatial hearing, including the precedence effect, is thought to depend on the auditory cortex. Therefore we tested the hypothesis that the activity of cortical neurons signals the perceived location of fused pairs of sounds. We recorded the unit responses of cortical neurons in areas A1 and A2 of anesthetized cats. Single broadband clicks were presented from various frontal locations. Paired clicks were presented with various ISDs and ISLDs from two loudspeakers located 50 degrees to the left and right of midline. Units typically responded to single clicks or paired clicks with a single burst of spikes. Artificial neural networks were trained to recognize the spike patterns elicited by single clicks from various locations. The trained networks were then used to identify the locations signaled by unit responses to paired clicks. At ISDs of 1-4 ms, unit responses typically signaled locations near that of the leading source in agreement with localization dominance. Nonetheless the responses generally exhibited a substantial undershoot; this finding, too, accorded with psychophysical measurements. As the ISD was decreased from ~0.4 to 0 ms, network estimates typically shifted from the leading location toward the midline in agreement with summing localization. Furthermore a superposed ISLD shifted network estimates toward the more intense source, reaching an asymptote at an ISLD of 15-20 dB. To allow quantitative comparison of our physiological findings to psychophysical results, we performed human psychophysical experiments and made acoustical measurements from the ears of cats and humans. After accounting for the difference in head size between cats and humans, the responses of cortical units usually agreed with the responses of human listeners, although a sizable minority of units defied psychophysical expectations.     

A neuronal correlate of the precedence effect is associated with spatial selectivity in the barn owl's auditory midbrain

Sound localization in echoic conditions depends on a precedence effect (PE), in which the first arriving sound dominates the perceived location of later reflections. Previous studies have demonstrated neurophysiological correlates of the PE in several species, but the underlying mechanisms remain unknown. The present study documents responses of space-specific neurons in the barn owl's inferior colliculus (IC) to stimuli simulating direct sounds and reflections that overlap in time at the listener's ears. Responses to 100-ms noises with lead-lag delays from 1 to 100 ms were recorded from neurons in the space-mapped subdivisions of IC in anesthetized owls (N2O/isofluorane). Responses to a target located at a unit's best location were usually suppressed by a masker located outside the excitatory portion of the spatial receptive field. The least spatially selective units exhibited temporally symmetric effects, in that the amount of suppression was the same whether the masker led or lagged. Such effects mirror the alteration of localization cues caused by acoustic superposition of leading and lagging sounds. In more spatially selective units, the suppression was often temporally asymmetric, being more pronounced when the masker led. The masker often evoked small changes in spatial tuning that were not related to the magnitude of suppressive effects. The association of temporally asymmetric suppression with spatial selectivity suggests that this property emerges within IC, and not at earlier stages of auditory processing. Asymmetric suppression reduces the ability of highly spatially selective neurons to encode the location of lagging sounds, providing a possible basis for the PE.     

Spectral cues explain illusory elevation effects with stereo sounds in cats

Mammals localize sound sources in azimuth based on two binaural cues, interaural differences in the time of arrival and level of the sounds at the ears. In contrast, the cue for elevation is based on patterns of the broadband power spectra at each ear that result from the direction-dependent acoustic filtering properties of the head and pinnae. Although the exact form of this "spectral shape" cue is unknown, most attention has been directed toward a prominent direction-dependent energy minimum, or "notch," because its location in frequency, for both humans and cats, moves predictably from low to high as a source is moved from low to high elevations. However, there is little direct evidence that these spectral notches are important elevational cues in animals other than humans. Here we demonstrate a striking illusion in the localization of sounds in elevation by cats using stimulus configurations that elicit summing localization and the precedence effect that can be explained by spectral shape cues.     

Directional sensitivity of neurons in the primary auditory (AI) cortex of the cat to successive sounds ordered in time and space

Two transient sounds, considered as a conditioner followed by a probe, were delivered successively from the same or different direction in virtual acoustic space (VAS) while recording from single neurons in primary auditory cortex (AI) of cats under general anesthesia. Typically, the response to the probe sound was progressively suppressed as the interval between the two sounds (ISI) was systematically reduced from 400 to 50 ms, and the sound-source directions were within the cell's virtual space receptive field (VSRF). Suppression of the cell's discharge could be accompanied by an increase in response latency. In some neurons, the joint response to two sounds delivered successively was summative or facilitative at ISIs below about 20 ms. These relationships held throughout the VSRF, including those directions on or near the cell's acoustic axis where sounds often elicit the strongest response. The strength of suppression varied systematically with the direction of the probe sound when the ISI was fixed and the conditioning sound arrived from the cell's acoustic axis. Consequently a VSRF defined by the response to the lagging probe sound was progressively reduced in size when ISIs were shortened from 400 to 50 ms. Although the presence of a previous sound reduced the size of the VSRF, for many of these VSRFs a systematic gradient of response latency was maintained. The maintenance of such a gradient may provide a mechanism by which directional acuity remains intact in an acoustic environment containing competing acoustic transients.     

Multiple expression of glucose transporters in the lateral wall of the cochlear duct studied by quantitative real-time PCR assay

The precedence effect (PE) is thought to be beneficial for proper localization and perception of sounds. The majority of recent physiological studies focus on the neural discharges correlated with PE in the inferior colliculus (IC). Pentobarbital anesthesia is widely used in physiological studies. However, little is known of the effect of pentobarbital on the discharge of neurons in PE. Neuronal responses in the IC from 23 male SD rats were recorded by standard extracellular recording techniques following presentation of 4 ms white noise bursts, presented from either or both of two loud speakers, at different interstimulus delays (ISDs). The neural responses were recorded for off-line analysis before or after intraperitoneal administration of pentobarbital at a loading or maintenance dose. Data were assessed by one-way repeated measures analysis of variance and pairwise comparisons. When the ipsilateral stimuli were leading, pentobarbital at a loading dose significantly increased normalized response to lagging stimuli during recovery from anesthesia. However, it was not the case when the contralateral stimuli were leading. At a maintenance dose, the normalized response to lagging stimuli were significantly reduced, independent of whether contralateral or ipsilateral stimuli were leading. These data show that pentobarbital have no effect on the normalized response of leading stimuli but can prolong the recovery time of lagging stimuli to paired sources produced PE illusions, which was gradually attenuated during recovery from anesthesia. Thus, extracellular recording immediately after administration of pentobarbital should be avoided in physiological studies of neural correlates of PE.     

Mismatch negativity on the cone of confusion

Localization of sounds by the auditory system is based on the analysis of three sources of information: interaural level differences (ILD, caused by an attenuation of the sound as it travels to the more distant ear), interaural time differences (ITD, caused by the additional amount of time it takes for the sound to arrive at the more distant ear), and spectral cues (caused by direction-specific spectral filter properties of the pinnae). Although in a number of psychophysiological studies cortical processes of ITD and ILD analysis were investigated, there is hitherto no evidence on the cortical processing of spectral cues for sound localization. The objective of the present experiment was to test whether it is possible to observe electrophysiological correlates of sound localization based on spectral cues. In an auditory oddball experiment, 80 ms of broadband noise from varying free field locations were presented to inattentive participants. Mismatch negativities (MMNs) were observed for pairs of standards and location deviants located symmetrically with respect to the interaural axis. As interaural time and level differences are identical for such pairs of sounds, the observed MMNs most likely reflect cognitive processes of sound localization utilizing the spectral filter properties of the pinnae. MMN latencies suggest that sound localization based on spectral cues is slower than ITD- or ILD-based localization.     

Gender-specific association of the angiotensin converting enzyme gene with Alzheimer's disease

We measured human evoked magnetic fields to binaural sounds with an interaural time delay as a cue for auditory localization. By analyzing the topography of auditory-evoked magnetic fields in the middle-latency, we demonstrated that particular cortical regions represent the direction of sound localization by their activity level. Upon presenting a binaural sound, the first representations were found in the middle frontal region as well as the superior temporal region of the right hemisphere approximately 19 ms after the stimulation, but their patterns differed. Other cortical regions including the prefrontal and parietal spatial areas were affected within roughly 60 ms. The results showed that the right hemisphere is dominant even in the preattentive stage of auditory spatial processing of sounds from different directions.     

Neuromagnetic recordings reveal the temporal dynamics of auditory spatial processing in the human cortex

In an attempt to delineate the assumed 'what' and 'where' processing streams, we studied the processing of spatial sound in the human cortex by using magnetoencephalography in the passive and active recording conditions and two kinds of spatial stimuli: individually constructed, highly realistic spatial (3D) stimuli and stimuli containing interaural time difference (ITD) cues only. The auditory P1m, N1m, and P2m responses of the event-related field were found to be sensitive to the direction of sound source in the azimuthal plane. In general, the right-hemispheric responses to spatial sounds were more prominent than the left-hemispheric ones. The right-hemispheric P1m and N1m responses peaked earlier for sound sources in the contralateral than for sources in the ipsilateral hemifield and the peak amplitudes of all responses reached their maxima for contralateral sound sources. The amplitude of the right-hemispheric P2m response reflected the degree of spatiality of sound, being twice as large for the 3D than ITD stimuli. The results indicate that the right hemisphere is specialized in the processing of spatial cues in the passive recording condition. Minimum current estimate (MCE) localization revealed that temporal areas were activated both in the active and passive condition. This initial activation, taking place at around 100 ms, was followed by parietal and frontal activity at 180 and 200 ms, respectively. The latter activations, however, were specific to attentional engagement and motor responding. This suggests that parietal activation reflects active responding to a spatial sound rather than auditory spatial processing as such.     

Neural bases of an auditory illusion and its elimination in owls

Humans and owls localize sounds by detecting the arrival time disparity between the ears. Both species determine the interaural time difference by finding the delay necessary to match the leading signal with the lagging one. This method produces ambiguity with periodic signals, because the two signals can be matched by delaying either one or the other. As predicted, owls localized periodic signals in illusory directions, whereas they always perceived the real source when signal bandwidth exceeded a certain value. This bandwidth also enabled higher-order auditory neurons to discriminate between real and illusory sources.     

Neural correlates of the precedence effect in the inferior colliculus: effect of localization cues

The precedence effect (PE) is an auditory phenomenon involved in suppressing the perception of echoes in reverberant environments, and is thought to facilitate accurate localization of sound sources. We investigated physiological correlates of the PE in the inferior colliculus (IC) of anesthetized cats, with a focus on directional mechanisms for this phenomenon. We used a virtual space (VS) technique, where two clicks (a "lead" and a "lag") separated by a brief time delay were each filtered through head-related transfer functions (HRTFs). For nearly all neurons, the response to the lag was suppressed for short delays and recovered at long delays. In general, both the time course and the directional patterns of suppression resembled those reported in free-field studies in many respects, suggesting that our VS simulation contained the essential cues for studying PE phenomena. The relationship between the directionality of the response to the lead and that of its suppressive effect on the lag varied a great deal among IC neurons. For a majority of units, both excitation produced by the lead and suppression of the lag response were highly directional, and the two were similar to one another. For these neurons, the long-lasting inhibitory inputs thought to be responsible for suppression seem to have similar spatial tuning as the inputs that determine the excitatory response to the lead. Further, the behavior of these neurons is consistent with psychophysical observations that the PE is strongest when the lead and the lag originate from neighboring spatial locations. For other neurons, either there was no obvious relationship between the directionality of the excitatory lead response and the directionality of suppression, or the suppression was highly directional whereas the excitation was not, or vice versa. For these neurons, the excitation and the suppression produced by the lead seem to depend on different mechanisms. Manipulation of the directional cues (such as interaural time and level differences) contained in the lead revealed further dissociations between excitation and suppression. Specifically, for about one-third of the neurons, suppression depended on different directional cues than did the response to the lead, even though the directionality of suppression was similar to that of the lead response when all cues were present. This finding suggests that the inhibitory inputs causing suppression may originate in part from subcollicular auditory nuclei processing different directional cues than the inputs that determine the excitatory response to the lead. Neurons showing such dissociations may play an important role in the PE when the lead and the lag originate from very different directions.     

Blind subjects process auditory spectral cues more efficiently than sighted individuals

The goal of the present study was to investigate how monaural sound localization on the horizontal plane in blind humans is affected by manipulating spectral cues. As reported in a previous study (Lessard et al. 1998), blind subjects are able to calibrate their auditory space despite their congenital lack of vision. Moreover, the performance level of half of the blind subjects was superior to that of sighted subjects under monaural listening conditions. Here, we first tested ten blind subjects and five controls in free-field (1) binaural and (2) monaural sound localization tasks. Results showed that, contrary to controls and half the blind subjects, five of the blind listeners were able to localize the sounds with one ear blocked. The blind subjects who showed good monaural localization performances were then re-tested in three additional monaural tasks, but we manipulated their ability to use spectral cues to carry out their discrimination. These subjects thus localized these same sounds: (3) with acoustical paste on the pinna, (4) with high-pass sounds and unobstructed pinna and (5) with low-pass sounds and unobstructed pinna. A significant increase in localization errors was observed when their ability to use spectral cues was altered. We conclude that one of the reasons why some blind subjects show supra-normal performances might be that they more effectively utilize auditory spectral cues.     

Visual motion perception induced by sounds in vertical plane

The alternation of sounds in the left and right ears induces motion perception of a static visual stimulus (SIVM: Sound-Induced Visual Motion). In this case, binaural cues were of considerable benefit in perceiving locations and movements of the sounds. The present study investigated how a spectral cue – another important cue for sound localization and motion perception – contributed to the SIVM. In experiments, two alternating sound sources aligned in the vertical plane were presented, synchronized with a static visual stimulus. We found that the proportion of the SIVM and the magnitude of the perceived movements of the static visual stimulus increased with an increase of retinal eccentricity (1.875–30°), indicating the influence of the spectral cue on the SIVM. These findings suggest that the SIVM can be generalized to the whole two dimensional audio–visual space, and strongly imply that there are common neural substrates for auditory and visual motion perception in the brain.     

What and where in human audition: selective deficits following focal hemispheric lesions

A sound that we hear in a natural setting allows us to identify the sound source and localize it in space. The two aspects can be disrupted independently as shown in a study of 15 patients with focal right-hemispheric lesions. Four patients were normal in sound recognition but severely impaired in sound localization, whereas three other patients had difficulties in recognizing sounds but localized them well. The lesions involved the inferior parietal and frontal cortices, and the superior temporal gyrus in patients with selective sound localization deficit; and the temporal pole and anterior part of the fusiform, inferior and middle temporal gyri in patients with selective recognition deficit. These results suggest separate cortical processing pathways for auditory recognition and localization. Electronic Publication     

Delay-tuned combination-sensitive neurons in the auditory cortex of the vocalizing mustached bat

1. FM-FM neurons in the auditory cortex of the mustached bat are sensitive to a pair of frequency-modulated (FM) sounds that simulates an FM component of the orientation sound and an FM component of the echo. These neurons are tuned to particular delays between the two FM components, suggesting an encoding of target range information. The response properties of these FM-FM neurons, however, have previously been studied only with synthesized orientation sounds and echoes delivered from a loud-speaker as substitutes for the bat's own orientation sounds and corresponding echoes. In this study, the combination sensitivity and delay tuning of FM-FM neurons were examined while the bat was actively vocalizing. 2. When the bat produced orientation sounds in an anechoic environment, or synthesized single FM echoes were delivered to a silent bat, the FM-FM neurons showed weak or no response. In contrast, when synthesized FM echoes were delivered with a particular delay from the FM component of the vocalized orientation sounds, the FM-FM neurons exhibited strong facilitative responses. 3. In both the vocalizing bats and the silent bats with substituted synthesized orientation sounds, all FM-FM neurons tested responded preferentially to the same echo harmonic (FM2, FM3, or FM4). 4. In vocalizing bats, FM-FM neurons showed maximum response to an echo FM component delivered with a particular delay (best delay) from an FM component in the orientation sound. Best delays measured with vocalized orientation sounds were nearly the same as those measured with synthesized orientation sounds. 5. The equivalent effect of a vocalized orientation sound and a synthesized FM1 component on the activity of FM-FM neurons indicates that, during echolocation, the FM1 component in the vocalized orientation sound stimulates the auditory system and conditions the FM-FM neurons to be sensitive to echoes with particular delays from the vocalized orientation sounds. 6. The amount of vocal self-stimulation to the inner ear by the bat's own vocalized sounds was measured by recording cochlear microphonic potentials (CMs). Spectral analysis of CM indicated that the amount of vocal self-stimulation by each harmonic of an orientation sound was equivalent to a sound of 70 dB sound pressure level (SPL) for the first harmonic (H1), 91 dB SPL for H2, 83 dB SPL for H3, and 70 dB SPL for H4, when the amplitude of the vocalized sound was 117 dB SPL at 5 cm in front of the bat's mouth.     

Ultrafast tracking of sound location changes as revealed by human auditory evoked potentials

The rapid discrimination of auditory location information enables grouping and selectively attending to specific sound sources. The typical indicator of auditory change detection is the mismatch negativity (MMN) occurring at a latency of about 100-250 ms. However, recent studies have revealed the existence of earlier markers of frequency deviance detection in the middle-latency response (MLR). Here, we measured the MLR and MMN to changes in sound location. Clicks were presented in either the left or right hemifields during oddball (rare 30°-shifts in location), reversed oddball, and control (sounds occurring equiprobably from five locations) conditions. Clicks at deviant locations elicited an MMN and an enhanced Na component of the MLR peaking at 20 ms compared to clicks at standard or control locations. Whereas MMN was not significantly lateralized, the Na effect showed a contralateral dominance. These findings indicate that, also for sound location changes, early detection processes exist upstream of MMN.     

Midline and lateral field sound localization in the ferret (Mustela putorius): contribution of the superior olivary complex.

1. The ability of ferrets to localize sound in space was determined before and after unilateral or bilateral lesions of the superior olivary complex (SOC). Lesions were made by pressure injection of kainic acid into the SOC through a stereotaxically positioned glass micropipette. The lesions destroyed the cell bodies in the superior olive without disrupting fibers of passage in the trapezoid body or other pathways in the auditory brain stem. The integrity of fibers was demonstrated by protargol staining of axonal processes and by the retrograde transport of horseradish peroxidase (HRP) from the inferior colliculus to other auditory brain stem nuclei. Behavioral tests were carried out separately for sound localization at midline and lateral field positions. Minimum audible angles were determined for single 45-ms noise bursts presented through paired loudspeakers positioned symmetrically around 0, -60, and +60 degrees azimuth. 2. Four ferrets received complete lesions of the left SOC, and two received complete lesions of the right SOC. In general, unilateral destruction of the superior olive resulted in impairments in sound localization in both left and right lateral fields. In some cases, deficits were also apparent on midline. Four additional animals received unilateral lesions that spared cells within the SOC. In most cases, deficits were apparent despite incomplete lesions of the SOC. The pattern of deficits was generally consistent with that found in animals with complete lesions. Most animals had difficulty localizing sounds in the lateral fields. 3. Four animals received bilateral lesions of the SOC. Three had complete or near-complete destruction of the superior olive on one side of the brain with relatively minor damage on the other side. Each of these animals exhibited behavioral deficits that were particularly severe ipsilateral to the more extensively damaged superior olive. One animal with complete bilateral destruction of the SOC was incapable of sound localization, even with 2-s noise bursts. This animal, however, suffered severe motor impairments after surgery that might have contributed to the apparent inability to localize sound. 4. Two animals with kainic acid lesions that caused little or no damage to the SOC were still capable of high levels of performance in tests of sound localization and had no elevation in minimum audible angles. These cases served as controls for the possible effects of nonspecific brain damage and demonstrated that kainic acid injections per se resulted in no obvious deficits in our test situation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Genetic variation in the male courtship sound ofDrosophila littoralis

Drosophila littoralis males and females emit sounds during courtship by vibrating their wings. Genetic variation in the male courtship sound of this species was studied by analyzing the sounds of males of 42 fresh isofemale strains from three localities in Finland and those of several laboratory strains originating from Europe and Caucasus. Among the fresh strains, the mean number of sound cycles in a pulse varied from 12 to 17 cycles, the length of a pulse from 39 to 51 ms, the length of a sound cycle from 2.9 to 3.6 ms, and the length of an interpulse interval (ipi) from 280 to 400 ms. The sounds of the old laboratory strains differed from each other more than the sounds of the fresh strains. There was, however, no sign of geographic differentiation.This study was aided by funds from The Academy of Finland.