Psychophysical investigation of an auditory spatial illusion in cats: the precedence effect

The precedence effect (PE) describes several spatial perceptual phenomena that occur when similar sounds are presented from two different locations and separated by a delay. The mechanisms that produce the effect are thought to be responsible for the ability to localize sounds in reverberant environments. Although the physiological bases for the PE have been studied, little is known about how these sounds are localized by species other than humans. Here we used the search coil technique to measure the eye positions of cats trained to saccade to the apparent locations of sounds. To study the PE, brief broadband stimuli were presented from two locations, with a delay between their onsets; the delayed sound meant to simulate a single reflection. Although the cats accurately localized single sources, the apparent locations of the paired sources depended on the delay. First, the cats exhibited summing localization, the perception of a "phantom" sound located between the sources, for delays < +/-400 micros for sources positioned in azimuth along the horizontal plane, but not for sources positioned in elevation along the sagittal plane. Second, consistent with localization dominance, for delays from 400 micros to about 10 ms, the cats oriented toward the leading source location only, with little influence of the lagging source, both for horizontally and vertically placed sources. Finally, the echo threshold was reached for delays >10 ms, where the cats first began to orient to the lagging source on some trials. These data reveal that cats experience the PE phenomena similarly to humans.     

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.     

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.     

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.     

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.     

Spatial attention modulates sound localization in barn owls

Attentional influence on sound-localization behavior of barn owls was investigated in a cross-modal spatial cuing paradigm. After being cued to the most probable target side with a visual cuing stimulus, owls localized upcoming auditory target stimuli with a head turn toward the position of the sound source. In 80% of the trials, cuing stimuli pointed toward the side of the upcoming target stimulus (valid configuration), and in 20% they pointed toward the opposite side (invalid configuration). We found that owls initiated the head turns by a mean of 37.4 ms earlier in valid trials, i.e., mean response latencies of head turns were reduced by 16% after a valid cuing stimulus. Thus auditory stimuli appearing at the cued side were processed faster than stimuli appearing at the uncued side, indicating the influence of a spatial-selective attention mechanism. Turning angles were not different when owls turned their head toward a cued or an uncued location. Other types of attention influencing sound localization, e.g., a reduction of response latency as a function of the duration of cue-target delay, could not be observed. This study is the first attempt to investigate attentional influences on sound localization in an animal model.     

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.     

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.     

A developmental look at an auditory illusion: The precedence effect

Infants aged 2 and 6 months were tested with the precedence effect, an auditory phenomenon involving sound localization. Each infant was tested with two types of stimuli: sound from a single loudspeaker and precedence-effect sounds produced by the same sound put through two loudspeakers, with one output leading the other by 7 msec. Older infants localized precedence-effect stimuli as they did single-source stimuli, indicating that they perceived this phenomenon as expected. Two-month-olds turned their heads toward single-source sounds, but did not localize precedence-effect sounds, suggesting that that more difficult perceptual task had not been achieved at this age. In general, headturning toward sound proved far more difficult to elicit in younger infants. A click train was ineffective, but a tape-recorded human voice elicited above-chance low-level turning. The developmental changes in auditory behavior are discussed in terms of the rapid growth of the auditory cortex.     

Persistent perceptual delay for head movement onset relative to auditory stimuli of different durations and rise times

The perception of simultaneity between auditory and vestibular information is crucially important for maintaining a coherent representation of the acoustic environment whenever the head moves. It has been recently reported, however, that despite having similar transduction latencies, vestibular stimuli are perceived significantly later than auditory stimuli when simultaneously generated. This suggests that perceptual latency of a head movement is longer than a co-occurring sound. However, these studies paired a vestibular stimulation of long duration (~1 s) and of a continuously changing temporal envelope with a brief (10–50 ms) sound pulse. In the present study, the stimuli were matched for temporal envelope duration and shape. Participants judged the temporal order of the two stimuli, the onset of an active head movement and the onset of brief (50 ms) or long (1,400 ms) sounds with a square- or raised-cosine-shaped envelope. Consistent with previous reports, head movement onset had to precede the onset of a brief sound by about 73 ms in order for the stimuli to be perceived as simultaneous. Head movements paired with long square sounds (~100 ms) were not significantly different than brief sounds. Surprisingly, head movements paired with long raised-cosine sound (~115 ms) had to be presented even earlier than brief stimuli. This additional lead time could not be accounted for by differences in the comparison stimulus characteristics (temporal envelope duration and shape). Rather, differences between sound conditions were found to be attributable to variability in the time for head movement to reach peak velocity: the head moved faster when paired with a brief sound. The persistent lead time required for vestibular stimulation provides further evidence that the perceptual latency of vestibular stimulation is greater than the other senses.     

Dynamic shifts in the owl's auditory space map predict moving sound location

The optic tectum of the barn owl contains a map of auditory space. We found that, in response to moving sounds, the locations of receptive fields that make up the map shifted toward the approaching sound. The magnitude of the receptive field shifts increased systematically with increasing stimulus velocity and, therefore, was appropriate to compensate for sensory and motor delays inherent to auditory orienting behavior. Thus, the auditory space map is not static, but shifts adaptively and dynamically in response to stimulus motion. We provide a computational model to account for these results. Because the model derives predictive responses from processes that are known to occur commonly in neural networks, we hypothesize that analogous predictive responses will be found to exist widely in the central nervous system. This hypothesis is consistent with perceptions of stimulus motion in humans for many sensory parameters.     

Lights can reverse illusory directional hearing

Adding brief flashes of light to a train of auditory clicks [R. Hari, Illusory directional hearing in humans, Neurosci. Lett. 189 (1995) 29-30] can alter the sounds perceived location within the head. In an experimental procedure adopted from Hari [R. Hari, Illusory directional hearing in humans, Neurosci. Lett. 189 (1995) 29-30], 16 observers listened over headphones to 8 binaural clicks (i.e., 4 left-ear leading followed by 4 right-ear leading) separated by one of three ISIs (8, 64 and 120 ms), then reported the perceived location of each click-pair within the head. Flashing a light rightward across a CRT screen during temporally coincident click-pairs made observers report the location of the sounds in roughly equally spaced steps from left-to-right through the head. In contrast, light flashes originating on the right of the CRT and moving leftward reversed the perceived location of the clicks, so that the sound appeared to originate on the right side of the head and shift leftward. These effects were diminished when the first four lights were all presented on one side of the CRT and the last four lights were all presented on the other side of the CRT. This multimodal phenomenon occurs although the light was perceived external to the head while the sounds presented over headphones were perceived within the head.     

Stimulus duration and repetition rate influence newborns' head orientation toward sound

Three experiments evaluated the effects of stimulus duration and repetition rate on newborns' head orientation responses. In Experiment 1, 28 infants turned toward a 20-sec continuous rattle sound but not toward 14- and 500-msec rattle sounds. Signal energy as a possible explanation for the infants' difficulty orienting toward brief sounds was explored in Experiment 2. Twenty neonates did not turn toward a single 90 dB, 14-msec rattle sound, although a longer duration (10 sec) sound containing less energy (70 dB) did elicit reliable head orientation. In Experiment 3, 16 neonates heard trains of repeated 14-msec rattle sounds (2/sec, 1.3/sec, and 1/sec) lasting 10 sec as well as a 10-sec continuous rattle sound. They turned toward the most rapidly repeating brief sound and the continuous one, while the slowly repeating sounds elicited little head movement in any direction. These results suggest that newborns' head orientation is selectively deficient for brief sounds, that the difficulty does not result from lessened energy in the brief sounds, and that the efficacy of repeated brief sounds depends upon their repetition rates.     

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.     

Development of auditory localization in dogs: single source and precedence effect sounds

The development of auditory localization in dogs was investigated in a litter of 12 pups. Behavioral auditory localization consisted of orienting responses to dog vocalizations presented from loudspeakers 90 degrees to each side. Sounds were presented in two configurations, single source (only one loudspeaker) and precedence effect (both loudspeakers, with one slightly leading the other). Localization began around 16 days after birth, for single-source sounds. This is consistent with previous observations and with findings on dogs' auditory neural development. Single-source sounds were localized earlier during development than precedence-effect sounds. This ordering resembles findings on human infants and can be related to neuroanatomical investigations of mammalian brain structures mediating single source versus precedence effect localization.     

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.     

Sound localization behavior in ferrets: comparison of acoustic orientation and approach-to-target responses

Auditory localization experiments typically either require subjects to judge the location of a sound source from a discrete set of response alternatives or involve measurements of the accuracy of orienting responses made toward the source location. To compare the results obtained by both methods, we trained ferrets by positive conditioning to stand on a platform at the center of a circular arena prior to stimulus presentation and then approach the source of a broadband noise burst delivered from 1 of 12 loudspeakers arranged at 30 degrees intervals in the horizontal plane. Animals were rewarded for making a correct choice. We also obtained a non-categorized measure of localization accuracy by recording head-orienting movements made during the first second following stimulus onset. The accuracy of the approach-to-target responses declined as the stimulus duration was reduced, particularly for lateral and posterior locations, although responses to sounds presented in the frontal region of space and directly behind the animal remained quite accurate. Head movements had a latency of approximately 200 ms and varied systematically in amplitude with stimulus direction. However, the final head bearing progressively undershot the target with increasing eccentricity and rarely exceeded 60 degrees to each side of the midline. In contrast to the approach-to-target responses, the accuracy of the head orienting responses did not change much with stimulus duration, suggesting that the improvement in percent correct scores with longer stimuli was due, at least in part, to re-sampling of the acoustical stimulus after the initial head turn had been made. Nevertheless, for incorrect trials, head orienting responses were more closely correlated with the direction approached by the animals than with the actual target direction, implying that at least part of the neural circuitry for translating sensory spatial signals into motor commands is shared by these two behaviors.     

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.     

Combined auditory and visual stimuli facilitate head saccades in the barn owl (Tyto alba)

The barn owl naturally responds to an auditory or visual stimulus in its environment with a quick head turn toward the source. We measured these head saccades evoked by auditory, visual, and simultaneous, co-localized audiovisual stimuli to quantify multisensory interactions in the barn owl. Stimulus levels ranged from near to well above saccadic threshold. In accordance with previous human psychophysical findings, the owl's saccade reaction times (SRTs) and errors to unisensory stimuli were inversely related to stimulus strength. Auditory saccades characteristically had shorter reaction times but were less accurate than visual saccades. Audiovisual trials, over a large range of tested stimulus combinations, had auditory-like SRTs and visual-like errors, suggesting that barn owls are able to use both auditory and visual cues to produce saccades with the shortest possible SRT and greatest accuracy. These results support a model of sensory integration in which the faster modality initiates the saccade and the slower modality remains available to refine saccade trajectory.     

Distortions of auditory space during rapid head turns

Auditory localisation was examined using brief broadband sounds presented during rapid head turns to visual targets in the peripheral field. Presenting sounds during a rapid head movement will “smear” the acoustic cues to the sound’s location. During the early stages of a head turn, sound localisation accuracy was comparable to a no-turn control condition. However, significant localisation errors occurred when the probe sound was presented during the later part of a head turn. After correcting for head position, the estimate of lateral angle (horizontal position) in the front hemisphere was generally accurate. However, lateral angle estimates for positions in the rear hemisphere exhibited systematic errors that were especially large around the midline. Polar angle (elevation) perception remained robust, being comparable to no-turn controls whether tested early or late in the head turn. The results are interpreted in terms of a ‘multiple look’ strategy for calculating sound location, and the allocation of attention to the hemisphere containing the head-turn target.