Binaural interaction in the brain-stem auditory evoked potential: evidence for a delay line coincidence detection mechanism

The binaural interaction component (BIC) of the brain-stem auditory evoked potential (BAEP) was studied in 13 normally hearing adults by subtracting the response to binaural clicks from the algebraic sum of monaural responses. Eight or 16 electrodes on the head and neck were referred to a non-cephalic site, the binaural stimuli were delivered either simultaneously or with an inter-aural time difference (Δt) of 0.2–1.6 msec, and masking noise was presented to the non-stimulated ear.With simultaneous binaural clicks a BIC was identifiable in every subject, the most consistent peaks being a scalp-positive potential (P1) peaking approximately 0.2 msec after wave V and a scalp negativity (N1) 0.7 msec later. Similar potentials were identifiable in 6/7 subjects with Δt fo 0.4 msec, 5/7 at 0.8 msec but only 1/7 at 1.2 msec. This suggests that the BIC may be associated with sound localization mechanisms which are sensitive to a similar range of Δt. On increasing Δt from 0.0 to 0.8 msec, the BIC was progressively delayed by approximately half the inter-aural time difference, with no suggestion of increasing temporal dispersion. This supports the notion of a ‘delay line coincidence detection’ mechanism in which the BIC represents the output of binaurally responsive neurones, probably in the superior olivary complex, which are ‘tuned’ to a particular Δt by the relative lengths of presynaptic axons relaying input from either ear.The distribution of the BIC in sagittal and coronal electrode chains was compared with that of binaural BAEP components I–VI and found to bear the closest resemblance to wave IV. It is suggested that both components may originate largely in the lateral lemnisci.     

Scalp potentials following sudden coherence and discoherence of binaural noise and change in the inter-aural time difference: a specific binaural evoked potential or a “mismatch” response?

When uncorrelated random noise signals presented to the two ears suddenly become identical (coherent), a centrally located sound image is abruptly perceived and long latency scalp potentials are evoked. When the same signals are presented monaurally there is no perceived change and no potentials are evoked: hence the response must be purely a function of the binaural interaction.P70, N130 and P220 components were consistently recorded to both coherence and discoherence. N130 was usually largest at Fz and P220 at Cz. No potentials of shorter latency were identified, even after averaging 5000 or more sweeps. When the noise became coherent with an inter-aural time difference (δT) of ±0.5 msec (giving rise to an off-centre sound image), the responses were of slightly longer latency and showed no significant asymmetries between C3 and C4. In binaurally coherent noise, δT changes of ±0.5 or ±1.0 msec evoked similar responses which showed no significant asymmetries on the scalp. N130 was of longer latency when δT was changed from ±0.5 msec to zero, as compared with the converse change.In view of the similarity of all these responses it is considered unlikely that they were due to specific populations of binaurally responsive cortical neurones. The N130 and P220 components are thought to be non-specific potentials which are elicited by amy perceptible change in steady auditory stimulus conditions, due to a “mismatch” between the stimulus and the contents of a short-term auditory memory.     

Role of the caudate nucleus in differentiating spatially separated acoustic signals in the dog

In tests on dogs the influence has been studied of bilateral electrolytic lesion of the caudate nuclei heads on realization of acquired conditioned instrumental defensive reactions to spatially separated sound signals (clicks series) under dichotic stimulation. It is shown that caudatectomy does not influence the dogs differentiation of the side of monaural sound stimulation, but leads to their absolute disability for a long time to differentiate right- and left-side positions of the sound image, modelled by changes in interaural difference in time of sound signal arrival at binaural stimulation.     

Role of phasic changes in sound signal in localization of auditory image

The work presents experimental data on certain changes in electrical responses of the auditory system's midbrain centre in a contraphasic binaural presentation of sound impulse series. Neuronal cortical activity is selective in respect to dynamic interaural changes of signals' phasic spectre which may serve as a basis for the mechanisms of localising a moving source of sound. Human auditory evoked potentials reveal a manifestation of memorizing the auditory image movement direction as shown by appearance of stimuli deviant from standard mismatch negativity.     

Similar Impacts of the Interaural Delay and Interaural Correlation on Binaural Gap Detection

The subjective representation of the sounds delivered to the two ears of a human listener is closely associated with the interaural delay and correlation of these two-ear sounds. When the two-ear sounds, e.g., arbitrary noises, arrive simultaneously, the single auditory image of the binaurally identical noises becomes increasingly diffuse, and eventually separates into two auditory images as the interaural correlation decreases. When the interaural delay increases from zero to several milliseconds, the auditory image of the binaurally identical noises also changes from a single image to two distinct images. However, measuring the effect of these two factors on an identical group of participants has not been investigated. This study examined the impacts of interaural correlation and delay on detecting a binaurally uncorrelated fragment (interaural correlation = 0) embedded in the binaurally correlated noises (i.e., binaural gap or break in interaural correlation). We found that the minimum duration of the binaural gap for its detection (i.e., duration threshold) increased exponentially as the interaural delay between the binaurally identical noises increased linearly from 0 to 8 ms. When no interaural delay was introduced, the duration threshold also increased exponentially as the interaural correlation of the binaurally correlated noises decreased linearly from 1 to 0.4. A linear relationship between the effect of interaural delay and that of interaural correlation was described for listeners participating in this study: a 1 ms increase in interaural delay appeared to correspond to a 0.07 decrease in interaural correlation specific to raising the duration threshold. Our results imply that a tradeoff may exist between the impacts of interaural correlation and interaural delay on the subjective representation of sounds delivered to two human ears.     

Forecast ability of the auditory system during perception of gradually or abruptly moving short sound images

The ability to localize endpoints of sound image trajectories was studied in comparison with stationary sound image positions. Sound images moved either gradually or abruptly to the left or right from the head midline. Different types of sound image movement were simulated by manipulating the interaural time delay. Subjects were asked to estimate the position of the virtual sound source, using the graphic tablet. It was revealed that the perceived endpoints of the moving sound image trajectories, like stationary stimulus positions, depended on the interaural time delay. The perceived endpoints of the moving sound images simulated by stimuli with the final interaural time delay lower than 200 micros were displaced further from the head midline as compared to stationary stimuli of the same interaural time delays. This forward displacement of the perceived position of the moving target can be considered as "representational momentum" and can be explained by mental extrapolation of the dynamic information, which is necessary for successive sensorimotor coordination. For interaural time delays above 400 micros, final positions of gradually and abruptly moving sound sources were closer to the head midline than corresponding stationary sound image position. When comparing the results of both duration conditions, it was shown that in case of longer stimuli the endpoints of gradually moving sound images were lateralized further from the head midline for interaural time delays above 400 micros.     

Binaural disparity cues available to the barn owl for sound localization

1. Bilateral recording of cochlear potentials was used to measure the variations in interaural time differences (ITDs) and interaural intensity differences (IIDs) as a free-field auditory stimulus was moved to different positions around a barn owl's head. 2. ITD varied smoothly with stimulus azimuth across a broad frequency range. 3. ITD varied minimally with stimulus elevation, except at extreme angles from the horizontal. 4. IID varied with both stimulus elevation and stimulus azimuth. Lower frequencies were more sensitive to variations in azimuth, whereas higher frequencies were more sensitive to variations in elevation. 5. The loci of spatial coordinates that form iso-IID contours and iso-ITD contours form a non-orthogonal grid that relates binaural disparity cues to sound location.     

Effects of binaural decorrelation on neural and behavioral processing of interaural level differences in the barn owl (Tyto alba)

The effect of binaural decorrelation on the processing of interaural level difference cues in the barn owl (Tyto alba) was examined behaviorally and electrophysiologically. The electrophysiology experiment measured the effect of variations in binaural correlation on the first stage of interaural level difference encoding in the central nervous system. The responses of single neurons in the posterior part of the ventral nucleus of the lateral lemniscus were recorded to stimulation with binaurally correlated and binaurally uncorrelated noise. No significant differences in interaural level difference sensitivity were found between conditions. Neurons in the posterior part of the ventral nucleus of the lateral lemniscus encode the interaural level difference of binaurally correlated and binaurally uncorrelated noise with equal accuracy and precision. This nucleus therefore supplies higher auditory centers with an undegraded interaural level difference signal for sound stimuli that lack a coherent interaural time difference. The behavioral experiment measured auditory saccades in response to interaural level differences presented in binaurally correlated and binaurally uncorrelated noise. The precision and accuracy of sound localization based on interaural level difference was reduced but not eliminated for binaurally uncorrelated signals. The observation that barn owls continue to vary auditory saccades with the interaural level difference of binaurally uncorrelated stimuli suggests that neurons that drive head saccades can be activated by incomplete auditory spatial information.     

Avian interaural canal enhances interaural delay

Summary Using a simple model of the birds' binaural pressure difference acoustic receivers it was predicted that the interaural delay achieved by birds at low frequencies is far greater than that of mammals with a similar head-size. This was upheld when interaural delay was recorded, between the cochlear microphonics, for six species. Stimulus positions were varied over the azimuthal range from the frontal midline to the interaural axis. Predicted delays were frequency dependent (higher frequency, smaller delay), as were the actual delays, and the magnitude of the measured delays were comparable with predictions. Delays measured at high frequencies were close to those expected from pathlength around the head, but delays measured at low frequencies could be more than three times this expectation. This finding raises the possibility that interaural delay may be a useful localization cue in birds, even for those species with very small heads, since the large delays at low frequencies are sufficient to provide a physiological cue to azimuth.     

Echoic Memory: Investigation of Its Temporal Resolution by Auditory Offset Cortical Responses

Previous studies showed that the amplitude and latency of the auditory offset cortical response depended on the history of the sound, which implicated the involvement of echoic memory in shaping a response. When a brief sound was repeated, the latency of the offset response depended precisely on the frequency of the repeat, indicating that the brain recognized the timing of the offset by using information on the repeat frequency stored in memory. In the present study, we investigated the temporal resolution of sensory storage by measuring auditory offset responses with magnetoencephalography (MEG). The offset of a train of clicks for 1 s elicited a clear magnetic response at approximately 60 ms (Off-P50m). The latency of Off-P50m depended on the inter-stimulus interval (ISI) of the click train, which was the longest at 40 ms (25 Hz) and became shorter with shorter ISIs (2.5∼20 ms). The correlation coefficient r² for the peak latency and ISI was as high as 0.99, which suggested that sensory storage for the stimulation frequency accurately determined the Off-P50m latency. Statistical analysis revealed that the latency of all pairs, except for that between 200 and 400 Hz, was significantly different, indicating the very high temporal resolution of sensory storage at approximately 5 ms.     

The reflection of the simulated movement of a sound source in the evoked potentials of the inferior colliculus in the cat

EP series from the cat's inferior colliculus were recorded following binaural stimulation with click series imitating sound source movement due to variation of the interaural time delay (and thus evoking in man the sensation of the moving fused auditory image, FI). The "movement effect" was evaluated as the change in the EP amplitude during the series. The movement effect itself as well as its predominance under conditions of the ipsilateral FI movement as compared to those of the contralateral movement, proved to be connected with greater effectiveness of the contralateral stimulation relative the ipsilateral one.     

Localization of a sum of acoustic signals in air by the northern fur seal]

The localization of a sum of acoustic signals by two northern fur seals in air depending on sound parameters was investigated using the method of instrumental conditioned reflexes with food reinforcement. It was found that sound perception of northern fur seal proceeds by the binaural mechanism. The time/intensity interchange coefficient was 570 microseconds/dB for series of clicks (with amplitude maximum at 1 kHz) and 250 microseconds/dB for tonal impulses with a frequency of 1 kHz. With click amplitudes being equal, the number of approaches of the animal to the source of the first signal reached a 75% level at a delay of the second signal 0.07 ms (the minimum delay); with a delay of 6 ms (the maximum delay) and more, the fur seal, probably hears two separate signals. The minimum delay depended little on the duration of tonal impulses (with a frequency of 1 kHz) and was 0.3-0.7 ms; the maximum delay was 9-11 ms for tonal impulses with a duration of 3 ms and 37-40 ms with impulse duration 20 ms. The precedence effect became apparent at a greater delay for smooth fronts of impulses than for rectangular fronts.     

Forward masking in the evoked responses of the guinea pig auditory cortex: effects of variation of the interaural time and phase differences

In anaesthesized guinea pigs the evoked potentials of the auditory cortex were studied in a forward masking paradigm. In-phase and out-of-phase binaurally presented clicks with interaural time delay (ITD) were used as masker, in-phase click with ITD = 0 served as probe signal. Addition of the masking stimulus suppressed the probe-evoked response that followed the masker. The magnitude of the suppression correlated with the amount of the masker-evoked response: an increase in masker-evoked excitation caused a greater reduction in probe response magnitude. Amplitude of masker-evoked response was seen to be a monotonic or non-monotonic function of ITD. The non-monotonic response exhibited a sensitivity to the interaural phase differences when in-phase and out-of-phase maskers were presented, and showed the tendency to be periodic function of ITD in the expanded range of ITD values. Phase-sensitive responses differed in recovery time following the in-phase and out-of-phase masking stimuli. At near-threshold levels of a forward masker an enhancement of the probe-evoked response was observed.     

Three-channel Lissajous' trajectory of the binaural interaction components in human auditory brain-stem evoked potentials

The 3-channel Lissajous' trajectory (3-CLT) of the binaural interaction components (BI) in auditory brain-stem evoked potentials (ABEPs) was derived from 17 normally hearing adults by subtracting the response to binaural clicks (B) from the algebraic sum of monaural responses (L + R). ABEPs were recorded in response to 65 dB nHL, alternating polarity clicks, presented at a rate of 11/sec. A normative set of BI 3-CLT measures was calculated and compared with the corresponding measures of simultaneously recorded, single-channel vertex-left mastoid and vertex-neck derivations of BI and of ABEP L+R and B. 3-CLT measures included: apex latency, amplitude and orientation, as well as planar segment duration and orientation.The results showed 3 apices and associated planar segments (“Bd_II,” “Be” and “Bf”) in the 3-CLT of BI which corresponded in latency to the vertex-mastoid and vertex-neck peaks IIIn, V and VI of ABEP L + R and B. These apices corresponded in latency and orientation to apices of the 3-CLT of ABEP L + R and ABEP B. This correspondence suggests generators of the BI components between the trapezoid body and the inferior colliculus output. Durations of BI planar segments were approximately 1.0 msec. Apex amplitudes of BI 3-CLT were larger than the respective peak amplitudes of the vertex-mastoid and vertex-neck recorded BI, while their intersubject variabilities were comparable.     

Human middle-latency auditory evoked potentials: vertex and temporal components

We recorded middle-latency (20–70 msec) auditory evoked potentials (MLAEPs) to monaural and binaural clicks in 30 normal adults (ages 20–49 years) at 32 scalp locations all referred to a balanced non-cephalic reference. Our goal was to define the MLAEP components that were present at comparable latencies and comparable locations across the subject population. Group and individual data were evaluated both as topographic maps and as MLAEPs at selected electrode locations.Three major components occurred between 20 and 70 msec, two well-known peaks centered at the vertex, and one previously undefined peak focused over the posterior temporal area. Pa is a 29 msec positive peak centered at the vertex and present with both monaural and binaural stimulation, Pb is a 53 msec positive peak also centered at the vertex but seen consistently only with binaural and right ear stimulation. TP41 is a 41 msec positive peak focused over both temporal areas. TP41 has not been identified in previous MLAEP studies that concentrated on central scalp locations and/or used active reference electrode sites such as ears or mastoids.Available topographic, intracranial, pharmacologic, and lesion studies indicate that Pa, Pb and TP41 are of neural origin. Whether Pa and/or Pb are produced in Heschl's gyrus, primary auditory cortex, remains unclear. TP41 is probably produced by auditory cortex on the posterior lateral surface of the temporal lobe. It should prove of considerable value in experimental and clinical evaluation of higher level auditory function in particular and of cortical function in general.     

Temporal resolution of the Risso’s dolphin, Grampus griseus, auditory system

Toothed whales and dolphins (Odontocetes) are known to echolocate, producing short, broadband clicks and receiving the corresponding echoes, at extremely rapid rates. Auditory evoked potentials (AEP) and broadband click stimuli were used to determine the modulation rate transfer function (MRTF) of a neonate Risso’s dolphin, Grampus griseus, thus estimating the dolphin’s temporal resolution, and quantifying its physiological delay to sound stimuli. The Risso’s dolphin followed sound stimuli up to 1,000 Hz with a second peak response at 500 Hz. A weighted MRTF reflected that the animal followed a broad range of rates from 100 to 1,000 Hz, but beyond 1,250 Hz the animal’s hearing response was simply an onset/offset response. Similar to other mammals, the dolphin’s AEP response to a single stimulus was a series of waves. The delay of the first wave, PI, was 2.76 ms and the duration of the multi-peaked response was 4.13 ms. The MRTF was similar in shape to other marine mammals except that the response delay was among the fastest measured. Results predicted that the Risso’s dolphin should have the ability to follow clicks and echoes while foraging at close range.     

Effects of GABA-mediated inhibition on direction-dependent frequency tuning in the frog inferior colliculus

Earlier studies from our laboratory have shown that the frequency selectivity of neurons in the frog inferior colliculus is direction dependent. The goal of this study was to test the hypotheses that gamma-aminobutyric acid or GABA (but not glycine)-mediated synaptic inhibition was responsible for the direction-dependence in frequency tuning, and that GABA acted through creation of binaural inhibition. We performed single unit recordings and investigated the unit's free-field frequency tuning, and/or the unit's response to the interaural level differences (under dichotic stimulation), before and during local applications of antagonists specific to gamma-aminobutyric acid a and glycine receptors. Our results showed that application of bicuculline produced a broadening of free-field frequency tuning, and differential changes in free-field frequency tuning depending on sound direction, i.e., more pronounced at azimuths at which the unit exhibited narrower frequency tuning under the pre-drug condition, thereby typically abolishing direction dependence in tuning. Application of strychnine produced no change in frequency tuning. The results from dichotic stimulation further revealed that bicuculline typically elevated and/or flattened the unit's interaural-level-difference response function, indicating a reduction in the strength of binaural inhibition. Our study provides evidence that gamma-aminobutyric acid-mediated binaural inhibition is important for direction dependence in frequency tuning. Accepted: 24 July 1998     

The function of the medial superior olive in small mammals: temporal receptive fields in auditory analysis

Traditionally, the medial superior olive, a mammalian auditory brainstem structure, is considered to encode interaural time differences, the main cue for localizing low-frequency sounds. Detection of binaural excitatory and inhibitory inputs are considered as an underlying mechanism. Most small mammals, however, hear high frequencies well beyond 50 kHz and have small interaural distances. Therefore, they can not use interaural time differences for sound localization and yet possess a medial superior olive. Physiological studies in bats revealed that medial superior olive cells show similar interaural time difference coding as in larger mammals tuned to low-frequency hearing. Their interaural time difference sensitivity, however, is far too coarse to serve in sound localization. Thus, interaural time difference sensitivity in medial superior olive of small mammals is an epiphenomenon. We propose that the original function of the medial superior olive is a binaural cooperation causing facilitation due to binaural excitation. Lagging inhibitory inputs, however, suppress reverberations and echoes from the acoustic background. Thereby, generation of antagonistically organized temporal fields is the basic and original function of the mammalian medial superior olive. Only later in evolution with the advent of larger mammals did interaural distances, and hence interaural time differences, became large enough to be used as cues for sound localization of low-frequency stimuli. Accepted: 28 February 2000     

Coding interaural time differences at low best frequencies in the barn owl.

In birds and mammals, precisely timed spikes encode the timing of acoustic stimuli, and interaural acoustic disparities propagate to binaural processing centers. The Jeffress model proposes that these projections act as delay lines to innervate an array of coincidence detectors, every element of which has a different relative delay between its ipsilateral and contralateral excitatory inputs. Thus, interaural time difference (ITD) is encoded into the position of the coincidence detector whose delay lines best cancel out the acoustic ITD. Neurons of the avian nucleus laminaris and mammalian MSO phase-lock to both monaural and binaural stimuli but respond maximally when phase-locked spikes from each side arrive simultaneously, i.e. when the difference in the conduction delays compensates for the ITD. McAlpine et al. [Nat. Neurosci. 4 (2001) 396] identified an apparent difference between avian and mammalian ITD coding. In the barn owl, the maximum firing rate appears to encode ITD. This may not be the case for the guinea pig, where the steepest region of the function relating discharge rate to interaural time delay (ITD) is close to midline for all neurons, irrespective of best frequency (BF). These data suggest that low BF ITD sensitivity in the guinea pig is mediated by detection of a change in slope of the ITD function, and not by maximum rate. We review coding of low best frequency ITDs in barn owls and mammals and discuss whether there may be differences in the code used to signal ITD in mammals and birds.     

KILLER WHALE (ORCINUS ORCA) AUDITORY EVOKED POTENTIALS TO RHYTHMIC CLICKS

Temporal auditory mechanisms were measured in killer whales ( Orcinus orca ) by recording auditory evoked potentials (AEPs) to clicks. Clicks were presented at rates from 10/sec to 1,600/sec. At low rates, clicks evoked an AEP similar to the auditory brainstem response (ABR) of other odontocetes; however, peak latencies of the main waves were 3–3.7 msec longer than in bottlenose dolphins. Fourier analysis of the ABR showed a prominent peak at 300–400 Hz and a smaller one at 800–1,200 Hz. High-rate click presentation (more than 100/sec) evoked a rate-following response (RFR). The RFR amplitude depended little on rate up to 400/sec, decreased at higher rates and became undetectable at 1,120/sec. Fourier analysis showed that RFR fundamental amplitude dependence on frequency closely resembled the ABR spectrum. The fundamental could follow clicks to around 1,000/sec, although higher harmonics of lower rates could arise at frequencies as high as 1,200 Hz. Both RFR fundamental phase dependence on frequency and the response lag after a click train indicated an RFR group delay of around 7.5 msec. This corresponds to the latency of ABR waves PIII-NIV, which indicates the RFR originates as a rhythmic, overlapping ABR sequence. The data suggest the killer whale auditory system can follow high click rates, an ability that may have been selected for as a function of high-frequency hearing and the use of rapid clicks in echolocation.