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.     

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.     

Sensitivity of auditory cortical neurons to locations of signals and competing noise sources.

The present study examined cortical parallels to psychophysical signal detection and sound localization in the presence of background noise. The activity of single units or of small clusters of units was recorded in cortical area A2 of chloralose-anesthetized cats. Signals were 80-ms click trains that varied in location in the horizontal plane around the animal. Maskers were continuous broadband noises. In the focal masker condition, a single masker source was tested at various azimuths. In the diffuse masker condition, uncorrelated noise was presented from two speakers at +/-90 degrees lateral to the animal. For about 2/3 of units ("type A"), the presence of the masker generally reduced neural sensitivity to signals, and the effects of the masker depended on the relative locations of signal and masker sources. For the remaining 1/3 of units ("type B"), the masker reduced spike rates at low signal levels but often augmented spike rates at higher signal levels. Increases in spike rates of type B units were most common for signal sources in front of the ear contralateral to the recording site but tended to be independent of masker source location. For type A units, masker effects could be modeled as a shift toward higher levels of spike-rate- and spike-latency-versus-level functions. For a focal masker, the shift size decreased with increasing separation of signal and masker. That result resembled psychophysical spatial unmasking, i.e., improved signal detection by spatial separation of the signal from the noise source. For the diffuse masker condition, the shift size generally was constant across signal locations. For type A units, we examined the effects of maskers on cortical signaling of sound-source location, using an artificial-neural-network (ANN) algorithm. First, an ANN was trained to estimate the signal location in the quiet condition by recognizing the spike patterns of single units. Then we tested ANN responses for spike patterns recorded under various masker conditions. Addition of a masker generally altered spike patterns and disrupted ANN identification of signal location. That disruption was smaller, however, for signal and masker configurations in which the masker did not severely reduce units' spike rates. That result compared well with the psychophysical observation that listeners maintain good localization performance as long as signals are clearly audible.     

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.     

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.     

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.     

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.     

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.     

Characterization of the human auditory cortex by the neuromagnetic method

Summary Neuromagnetic studies show that the location of cortical activity evoked by modulated tones and by click stimuli in the steady state paradigm can be determined non-invasively with a precision of a few millimeters. The progression of locations for tones of increasing frequency establish an orderly tonotopic map in which the distance along the cortex varies as the logarithm of the frequency. The active region responding to clicks lies at a position that is consistent with this map if the stimulus is characterized by the frequency of the peak of its power spectrum. A latency of about 50 ms observed for the response to clicks is in close correspondance with a strong component of the transient response to an isolated click reported in the literature. Monaural stimulation of the ear contralateral to the hemisphere being monitored produces a latency which is about 8 ms shorter than stimulation of the ipsilateral ear, in agreement with previous studies of transient responses. The amplitudes of the responses for binaurally presented clicks for sleeping subjects is substantially diminished for repetition rates above 20 Hz but is enhanced for lower rates.Supported in part by Office of Naval Research Contract N00014-76-C-0568Supported by Consiglio Nazionale delle Ricerche and by Progetto Finalizzato Superconduttivitá — C.N.R.     

Effects of perceptual context on event-related brain potentials during auditory spatial attention

The effects of auditory spatial attention on event-related brain potentials (ERPs) were examined in situations that promoted stream segregation. Short and long noise bursts were presented at three azimuth locations and listeners were asked to respond to the longer sounds occurring at either the right- or left-most location. In the baseline condition, the three sound sources were evenly spaced apart. In the distractor clustering conditions, middle and far sounds were clustered. In the attended clustering conditions, middle and attended sounds were clustered. ERP indices of attention, isolated as negative difference (Nd) waves, were greater over the hemisphere contralateral to the attended location. Nd waves were also larger when the middle sounds were moved toward the far distractors, consistent with an object-based gradient of auditory attention in which higher order information provided by the perceptual context influences selective processing.     

Temporal discharge patterns evoked by rapid sequences of wide- and narrowband clicks in the primary auditory cortex of cat

The present study investigated neural responses to rapid, repetitive stimuli in the primary auditory cortex (A1) of cats. We focused on two important issues regarding cortical coding of sequences of stimuli: temporal discharge patterns of A1 neurons as a function of inter-stimulus interval and cortical mechanisms for representing successive stimulus events separated by very short intervals. These issues were studied using wide- and narrowband click trains with inter-click intervals (ICIs) ranging from 3 to 100 ms as a class of representative sequential stimuli. The main findings of this study are 1) A1 units displayed, in response to click train stimuli, three distinct temporal discharge patterns that we classify as regions I, II, and III. At long ICIs nearly all A1 units exhibited typical stimulus-synchronized response patterns (region I) consistent with previously reported observations. At intermediate ICIs, no clear temporal structures were visible in the responses of most A1 units (region II). At short ICIs, temporal discharge patterns are characterized by the presence of either intrinsic oscillations (at approximately 10 Hz) or a change in discharge rate that was a monotonically decreasing function of ICI (region III). In some A1 units, temporal discharge patterns corresponding to region III were absent. 2) The boundary between regions I and II (synchronization boundary) had a median value of 39.8 ms ICI ([25%, 75%] = [20.4, 58. 8] ms ICI; n = 131). The median boundary between regions II and III was estimated at 6.3 ms ([25%, 75%] = [5.2, 9.7] ms ICI; n = 47) for units showing rate changes (rate-change boundary). 3) The boundary values between different regions appeared to be relatively independent of stimulus intensity (at modest sound levels) or the bandwidth of the clicks used. 4) There is a weak correlation between a unit's synchronization boundary and its response latency. Units with shorter latencies appeared to also have smaller boundary values. And 5) based on these findings, we proposed a two-stage model for A1 neurons to represent a wide range of ICIs. In this model, A1 uses a temporal code for explicitly representing long ICIs and a rate code for implicitly representing short ICIs.     

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.     

Detecting violations of temporal regularities in waking and sleeping two-month-old infants

Correctly processing rapid sequences of sounds is essential for developmental milestones, such as language acquisition. We investigated the sensitivity of two-month-old infants to violations of a temporal regularity, by recording event-related brain potentials (ERPs) in an auditory oddball paradigm from 36 waking and 40 sleeping infants. Standard tones were presented at a regular 300 ms inter-stimulus interval (ISI). One deviant, otherwise identical to the standard, was preceded by a 100 ms ISI. Two other deviants, presented with the standard ISI, differed from the standard in their spectral makeup. We found significant differences between ERP responses elicited by the standard and each of the deviant sounds. The results suggest that the ability to extract both temporal and spectral regularities from a sound sequence is already functional within the first few months of life. The scalp distribution of all three deviant-stimulus responses was influenced by the infants’ state of alertness.     

Cortical representation of auditory space: information-bearing features of spike patterns

Previous studies have demonstrated that the spike patterns of cortical neurons vary systematically as a function of sound-source location such that the response of a single neuron can signal the location of a sound source throughout 360 degrees of azimuth. The present study examined specific features of spike patterns that might transmit information related to sound-source location. Analysis was based on responses of well-isolated single units recorded from cortical area A2 in alpha-chloralose-anesthetized cats. Stimuli were 80-ms noise bursts presented from loudspeakers in the horizontal plane; source azimuths ranged through 360 degrees in 20 degrees steps. Spike patterns were averaged across samples of eight trials. A competitive artificial neural network (ANN) identified sound-source locations by recognizing spike patterns; the ANN was trained using the learning vector quantization learning rule. The information about stimulus location that was transmitted by spike patterns was computed from joint stimulus-response probability matrices. Spike patterns were manipulated in various ways to isolate particular features. Full-spike patterns, which contained all spike-count information and spike timing with 100-micros precision, transmitted the most stimulus-related information. Transmitted information was sensitive to disruption of spike timing on a scale of more than approximately 4 ms and was reduced by an average of approximately 35% when spike-timing information was obliterated entirely. In a condition in which all but the first spike in each pattern were eliminated, transmitted information decreased by an average of only approximately 11%. In many cases, that condition showed essentially no loss of transmitted information. Three unidimensional features were extracted from spike patterns. Of those features, spike latency transmitted approximately 60% more information than that transmitted either by spike count or by a measure of latency dispersion. Information transmission by spike patterns recorded on single trials was substantially reduced compared with the information transmitted by averages of eight trials. In a comparison of averaged and nonaveraged responses, however, the information transmitted by latencies was reduced by only approximately 29%, whereas information transmitted by spike counts was reduced by 79%. Spike counts clearly are sensitive to sound-source location and could transmit information about sound-source locations. Nevertheless, the present results demonstrate that the timing of the first poststimulus spike carries a substantial amount, probably the majority, of the location-related information present in spike patterns. The results indicate that any complete model of the cortical representation of auditory space must incorporate the temporal characteristics of neuronal response patterns.     

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.     

Somatosensory evoked response source localization using actual cortical surface as the spatial constraint

Summary We localized right median nerve somatosensory evoked responses in a normal human subject using an equivalent dipole method applied to magnetic field recordings. High resolution, 3-dimensional MRI data were used to confine source locations to the cortical surface. Results localized in Brodmann area 3b corresponding to location of hand somatosensory cortex derived from direct brain stimulation studies. The solution was unique and total computational time for an exhaustive, brute-force search was small and the results realistic due to applied anatomical constraints. This study demonstrates feasibility of accurate, non-invasive, realistic localization of dynamic human cortical function using spatial constraints provided by MRI images.     

Role of cat primary auditory cortex for sound-localization behavior

Small lesions designed to completely destroy the cortical zone of representation of a restricted band of frequency were introduced within the primary auditory cortex (AI) in adult cats. Physiological mapping was used to guide placement of lesions. Sound-localization performance was evaluated prior to and after induction of these lesions in a seven-choice free-sound-field apparatus. All tested cats had profound contralateral hemifield deficits for the localization of brief tones at frequencies roughly corresponding to those whose representations were destroyed by the lesion. Sound-localization performance was normal at all other test frequencies. In a single adult cat, a massive lesion destroyed nearly all auditory cortex unilaterally, with only the representation of a narrow band of frequency within AI spared by the lesion. This cat had normal abilities for azimuthal sound localization across that frequency band but a profound contralateral deficit for the azimuthal localization of brief sounds at all other frequencies. Recorded sound-localization deficits were permanent. Localization of long-duration tones was not affected by a unilateral AI lesion. These studies indicate that, at least in cats, AI is necessary for normal binaural sound-localization behavior; among auditory cortical fields, AI is sufficient for normal binaural sound-localization behavior; sound-location representation is organized by frequency channel in the auditory forebrain; and AI in each hemisphere contributes to only contralateral free-sound-field location representation.     

Cortical activity patterns predict speech discrimination ability

Neural activity in the cerebral cortex can explain many aspects of sensory perception. Extensive psychophysical and neurophysiological studies of visual motion and vibrotactile processing show that the firing rate of cortical neurons averaged across 50-500 ms is well correlated with discrimination ability. In this study, we tested the hypothesis that primary auditory cortex (A1) neurons use temporal precision on the order of 1-10 ms to represent speech sounds shifted into the rat hearing range. Neural discrimination was highly correlated with behavioral performance on 11 consonant-discrimination tasks when spike timing was preserved and was not correlated when spike timing was eliminated. This result suggests that spike timing contributes to the auditory cortex representation of consonant sounds.     

Sound localization in newborn human infants

Newborns' localization of sounds was examined in two experiments that utilized different psychophysical procedures and imposed different task demands. The results of both experiments were consistent in indicating that neonates not only differentiate the hemifield of a sound source but have some capacity to localize a sound within the hemifields. Adjustment of their initial head turn angle following a within-hemifield shift in location of an ongoing sound indicated that head orientation in neonates is elicited not only by sound onset but also by changes in location of an ongoing sound. Thus, multiple stimulus parameters impact on this neonatal response. Results are related to research on sound localization in older infants, and discussed in light of early development of the central auditory system.©1994 John Wiley & Sons, Inc.