Detection Of Interaural Time Differences Research Articles

Principal neuron diversity in the murine lateral superior olive supports multiple sound localization strategies and segregation of information in higher processing centers

Principal neurons (PNs) of the lateral superior olive nucleus (LSO) in the brainstem of mammals compare information between the two ears and enable sound localization on the horizontal plane. The classical view of the LSO is that it extracts ongoing interaural level differences (ILDs). Although it has been known for some time that LSO PNs have intrinsic relative timing sensitivity, recent reports further challenge conventional thinking, suggesting the major function of the LSO is detection of interaural time differences (ITDs). LSO PNs include inhibitory (glycinergic) and excitatory (glutamatergic) neurons which differ in their projection patterns to higher processing centers. Despite these distinctions, intrinsic property differences between LSO PN types have not been explored. The intrinsic cellular properties of LSO PNs are fundamental to how they process and encode information, and ILD/ITD extraction places disparate demands on neuronal properties. Here we examine the ex vivo electrophysiology and cell morphology of inhibitory and excitatory LSO PNs in mice. Although overlapping, properties of inhibitory LSO PNs favor time coding functions while those of excitatory LSO PNs favor integrative level coding. Inhibitory and excitatory LSO PNs exhibit different activation thresholds, potentially providing further means to segregate information in higher processing centers. Near activation threshold, which may be physiologically similar to the sensitive transition point in sound source location for LSO, all LSO PNs exhibit single-spike onset responses that can provide optimal time encoding ability. As stimulus intensity increases, LSO PN firing patterns diverge into onset-burst cells, which can continue to encode timing effectively regardless of stimulus duration, and multi-spiking cells, which can provide robust individually integrable level information. This bimodal response pattern may produce a multi-functional LSO which can encode timing with maximum sensitivity and respond effectively to a wide range of sound durations and relative levels.

Discriminating spatialised speech in complex environments in multiple sclerosis

People with multiple sclerosis (pwMS) frequently present with deficits in binaural processing used for sound localization. This study examined spatial release from speech-on-speech masking in pwMS, which involves binaural processing and additional higher level mechanisms underlying streaming, such as spatial attention.26 pwMS with mild severity (Expanded Disability Status Scale score <3) and 20 age-matched controls listened via headphones to pre-recorded sentences from a standard list presented simultaneously with eight-talker babble. Virtual acoustic techniques were used to simulate sentences originating from 0°, 20°, or 50° on the interaural horizontal plane around the listener whilst babble was presented continuously at 0° azimuth, and participants verbally repeated the target sentence. In a separate task, two simultaneous sentences both containing a colour and number were presented, and participants were required to report the target colour and number. Both competing sentences could originate from 0°, 20°, or 50° on the azimuthal plane. Participants also completed a series of neuropsychological assessments, an auditory questionnaire, and a three-alternative forced-choice task that involved the detection of interaural time differences (ITDs) in noise bursts.Spatial release from masking was observed in both pwMS and controls, as response accuracy in the two speech discrimination tasks improved in the spatially separated conditions (20° and 50°) compared with the co-localised condition. However, pwMS demonstrated significantly less spatial release (18%) than controls (28%) when discriminating colour/number coordinates. At 50° separation, pwMS discriminated significantly fewer coordinates (77%) than controls (89%). In contrast, pwMS had similar performances to controls when sentences were presented in babble, and for the basic ITD discrimination task. Significant correlations between speech discrimination performance and standardized neuropsychological scores were observed across all spatial conditions.Our findings suggest that spatial hearing is likely to be implicated in pwMS, thereby affecting the perception of competing speech originating from various locations.

Revisiting the detection of interaural time differences in listeners with hearing loss.

Sensitivity to interaural time differences (ITDs) was measured in two groups of listeners, one with normal hearing and one with sensorineural hearing loss. ITD detection thresholds were measured for pure tones and for speech (a single word), in quiet and in the presence of noise. It was predicted that effects of hearing loss would be reduced for speech as compared to tones due to the redundancy of information across frequency. Thresholds were better overall, and the effects of hearing loss less pronounced, for speech than for tones. There was no evidence that effects of hearing loss were exacerbated in noise.

Neural Maps of Interaural Time Difference in the American Alligator: A Stable Feature in Modern Archosaurs.

Detection of interaural time differences (ITDs) is crucial for sound localization in most vertebrates. The current view is that optimal computational strategies of ITD detection depend mainly on head size and available frequencies, although evolutionary history should also be taken into consideration. In archosaurs, which include birds and crocodiles, the brainstem nucleus laminaris (NL) developed into the critical structure for ITD detection. In birds, ITDs are mapped in an orderly array or place code, whereas in the mammalian medial superior olive, the analog of NL, maps are not found. As yet, in crocodilians, topographical representations have not been identified. However, nontopographic representations of ITD cannot be excluded due to different anatomical and ethological features of birds and crocodiles. Therefore, we measured ITD-dependent responses in the NL of anesthetized American alligators of either sex and identified the location of the recording sites by lesions made after recording. The measured extracellular field potentials, or neurophonics, were strongly ITD tuned, and their preferred ITDs correlated with the position in NL. As in birds, delay lines, which compensate for external time differences, formed maps of ITD. The broad distributions of best ITDs within narrow frequency bands were not consistent with an optimal coding model. We conclude that the available acoustic cues and the architecture of the acoustic system in early archosaurs led to a stable and similar organization in today's birds and crocodiles, although physical features, such as internally coupled ears, head size, or shape, and audible frequency range, vary among the two groups.SIGNIFICANCE STATEMENT Interaural time difference (ITD) is an important cue for sound localization, and the optimal strategies for encoding ITD in neuronal populations are the subject of ongoing debate. We show that alligators form maps of ITD very similar to birds, suggesting that their common archosaur ancestor reached a stable coding solution different from mammals. Mammals and diapsids evolved tympanic hearing independently, and local optima can be reached in evolution that are not considered by global optimal coding models. Thus, the presence of ITD maps in the brainstem may reflect a local optimum in evolutionary development. Our results underline the importance of comparative animal studies and show that optimal models must be viewed in the light of evolutionary processes.

Microsecond interaural time differences of acoustic transients are decoded by inhibitory-excitatory interactions in neurons of the lateral superior olive

The lateral superior olive (LSO) in the auditory brainstem generates sensitivity to interaural level differences (ILD), an important cue for sound localization, by comparing excitatory (E) input from the ipsilateral ear with inhibitory (I) input from the contralateral ear. Large axosomatic synapses (e.g., calyx of Held) point to the importance of precise temporal processing, but that is not easily reconciled with ILD detection. We propose that the IE interaction allows detection of interaural time differences (ITD) of acoustic transients, to which humans are exquisitely sensitive. We obtained in vivo whole cell recordings of LSO and MSO neurons in the gerbil, while presenting monaural and binaural clicks. We found that ITD functions to clicks in the LSO are surprisingly steep, in contrast to MSO neurons, which are considered the main ITD detectors. Intracellular LSO recordings show EPSPs generated by the ipsilateral click and IPSPs by the contralateral click, where IPSPs often arrive earlier. Binaural spiking is maximally suppressed when the EPSP coincides with the falling slope rather than the peak of the IPSP. We conclude that LSO neurons are more sensitive to ITDs of transients than MSO neurons. This clarifies the importance of timing specializations in the LSO circuit.

A circuit for detection of interaural time differences in the nucleus laminaris of turtles.

The physiological hearing range of turtles is approximately 50-1000 Hz, as determined by cochlear microphonics ( Wever and Vernon, 1956a). These low frequencies can constrain sound localization, particularly in red-eared slider turtles, which are freshwater turtles with small heads and isolated middle ears. To determine if these turtles were sensitive to interaural time differences (ITDs), we investigated the connections and physiology of their auditory brainstem nuclei. Tract tracing experiments showed that cranial nerve VIII bifurcated to terminate in the first-order nucleus magnocellularis (NM) and nucleus angularis (NA), and the NM projected bilaterally to the nucleus laminaris (NL). As the NL received inputs from each side, we developed an isolated head preparation to examine responses to binaural auditory stimulation. Magnocellularis and laminaris units responded to frequencies from 100 to 600 Hz, and phase-locked reliably to the auditory stimulus. Responses from the NL were binaural, and sensitive to ITD. Measures of characteristic delay revealed best ITDs around ±200 μs, and NL neurons typically had characteristic phases close to 0, consistent with binaural excitation. Thus, turtles encode ITDs within their physiological range, and their auditory brainstem nuclei have similar connections and cell types to other reptiles.

Accurate Detection of Interaural Time Differences by a Population of Slowly Integrating Neurons

For localization of a sound source, animals and humans process the microsecond interaural time differences of arriving sound waves. How nervous systems, consisting of elements with time constants of about and more than 1 ms, can reach such high precision is still an open question. In this Letter we present a hypothesis and show theoretical and computational evidence that a rather large population of slowly integrating neurons with inhibitory and excitatory inputs (EI neurons) can detect minute temporal disparities in input signals which are significantly less than any time constant in the system.

Temporal weighting in binaural hearing: Distinct contributions of interaural time and level differences following sound onset.

The ability of a listener to make use of interaural level differences (ILDs) or envelope interaural time differences (ITDs) carried by modulated high-frequency sounds depends critically on the modulation period. Specifically, periods shorter than 4–5 ms substantially reduce the availability of ongoing cues, with the consequence that localization and discrimination increasingly rely on onset cues as the period decreases. Over the past several years, the authors have studied this dependence by measuring listeners’ detection of dynamic ITD and ILD, their temporal weighting of both cues during localization tasks, and their perception of simulated sources and echoes (i.e., precedence effects) carrying one or both cues. This presentation will review the results of those studies, which suggest that (a) onsets dominate processing of both cues at high rates; (b) postonset ILD sensitivity is better maintained, compared to postonset ITD, at high rates; (c) sensitivity to postonset ILD, but typically not ITD, exhibits a temporally increasing profile consistent with binaural temporal integration of that cue; and (d) maintained sensitivity to postonset ILD allows changes in that cue, but not ITD, to cause “breakdown” of precedence effects. [Work supported by NIH Grant Nos. R03 DC009482 and F31 DC010543, and NSF Grant No. IOB-0630338.]

Detection of Interaural Time Differences in the Alligator

The auditory systems of birds and mammals use timing information from each ear to detect interaural time difference (ITD). To determine whether the Jeffress-type algorithms that underlie sensitivity to ITD in birds are an evolutionarily stable strategy, we recorded from the auditory nuclei of crocodilians, who are the sister group to the birds. In alligators, precisely timed spikes in the first-order nucleus magnocellularis (NM) encode the timing of sounds, and NM neurons project to neurons in the nucleus laminaris (NL) that detect interaural time differences. In vivo recordings from NL neurons show that the arrival time of phase-locked spikes differs between the ipsilateral and contralateral inputs. When this disparity is nullified by their best ITD, the neurons respond maximally. Thus NL neurons act as coincidence detectors. A biologically detailed model of NL with alligator parameters discriminated ITDs up to 1 kHz. The range of best ITDs represented in NL was much larger than in birds, however, and extended from 0 to 1000 micros contralateral, with a median ITD of 450 micros. Thus, crocodilians and birds employ similar algorithms for ITD detection, although crocodilians have larger heads.

Auditory evoked magnetic fields in relation to interaural time delay and interaural correlation

The detection of interaural time differences (ITD) for sound localization depends on the similarity between the left and right ear signals, namely interaural correlation (IAC). Human localization performance deteriorates with decreasing IACs. In order to examine activity related to localization performance in the human cortex, auditory evoked magnetic fields to the ITD of bandpass noises with different IACs were analyzed. When the IAC was 0.95, the N1m amplitudes, i.e., the estimated equivalent current dipole moments, increased with increasing ITD. However the effect of ITD on the N1m amplitudes was not significant when the IAC was 0.5. When the ITD was 0.7 ms, the N1m amplitudes decreased with decreasing IACs. There were no systematic changes in the source location of N1m in the auditory cortex related to changes in ITD or IAC. The results suggest that localization performance is reflected in N1m amplitudes.

Cellular models of coincidence detection

The avian brainstem contains a circuit for detection of interaural time differences (ITDs). Bilateral projections from the cochlear nucleus magnocellularis (NM) form maps of ITD in the nucleus laminaris (NL). A computational model of a NL neuron investigates the cell’s ability to detect coincidences between ipsilateral and contralateral inputs. The model, constructed in the NEURON programming environment, is biophysically detailed and includes recent information on the distribution of high threshold potassium conductances in NL neurons. The role of dendritic processing is explored and emphasized, including the effects of dendrite size on postsynaptic potentials, parallel (multiple) dendritic processing, and the benefits of having dendrites at all. The model makes several predictions, some of which confirm those of a previous model [H. Agmon-Snir, C. E. Carr, and J. Rinzel, Nature 393, 268–272 (1998)]. Active potassium channels greatly increase the ability to detect coincidences at high frequencies. Rate-coded output is much more robust than vector-strength-coded output at distinguishing coincidences from partial coincidences. There is an optimal number of dendrites for a given stimulus frequency, dendritic length, and number of synaptic inputs. The most efficient dendritic length decreases with best frequency.

Effects of Interaural Decorrelation on Neural and Behavioral Detection of Spatial Cues

The detection of interaural time differences (ITDs) for sound localization critically depends on the similarity between the left and right ear signals (interaural correlation). We show that, like humans, owls can localize phantom sound sources well until the correlation declines to a very low value, below which their performance rapidly deteriorates. Decreasing interaural correlation also causes the response of the owl’s tectal auditory neurons to decline nonlinearly, with a rapid drop followed by a more gradual reduction. A detection-theoretic analysis of the statistical properties of neuronal responses could account for the variance of behavioral responses as interaural correlation is decreased. Finally, cross-correlation analysis suggests that low interaural correlations cause misalignment of cross-correlation peaks across different frequencies, contributing heavily to the nonlinear decline in neural and ultimately behavioral performance.

Delay Line Models of Sound Localization in the Barn Owl

The detection of interaural time differences underlies azimuthal sound localization in the barn owl. Sensitivity to these time differences arises in the brainstem nucleus laminaris. Auditory information reaches the nucleus laminaris via bilateral projections from the cochlear nucleus magnocellularis. The magnocellular inputs to the nucleus laminaris act as delay lines to create maps of interaural time differences. These delay lines are tapped by postsynaptic coincidence detectors that encode interaural time differences. The entire circuit, from the auditory nerve to the nucleus magnocellularis to the nucleus laminaris, is specialized for the encoding and preservation of temporal information. A mathematical model of this circuit (Grun et al., 1990) provides useful predictions

A circuit for detection of interaural time differences in the brain stem of the barn owl

Detection of interaural time differences underlies azimuthal sound localization in the barn owl Tyto alba. Axons of the cochlear nucleus magnocellularis, and their targets in the binaural nucleus laminaris, form the circuit responsible for encoding these interaural time differences. The nucleus laminaris receives bilateral inputs from the cochlear nucleus magnocellularis such that axons from the ipsilateral cochlear nucleus enter the nucleus laminaris dorsally, while contralateral axons enter from the ventral side. This interdigitating projection to the nucleus laminaris is tonotopic, and the afferents are both sharply tuned and matched in frequency to the neighboring afferents. Recordings of phase-locked spikes in the afferents show an orderly change in the arrival time of the spikes as a function of distance from the point of their entry into the nucleus laminaris. The same range of conduction time (160 mu sec) was found over the 700-mu m depth of the nucleus laminaris for all frequencies examined (4-7.5 kHz) and corresponds to the range of interaural time differences available to the barn owl. The estimated conduction velocity in the axons is low (3-5 m/sec) and may be regulated by short internodal distances (60 mu m) within the nucleus laminaris. Neurons of the nucleus laminaris have large somata and very short dendrites. These cells are frequency selective and phase-lock to both monaural and binaural stimuli. The arrival time of phase-locked spikes in many of these neurons differs between the ipsilateral and contralateral inputs. When this disparity is nullified by imposition of an appropriate interaural time difference, the neurons respond maximally. The number of spikes elicited in response to a favorable interaural time difference is roughly double that elicited by a monaural stimulus. Spike counts for unfavorable interaural time differences fall well below monaural response levels. These findings indicate that the magnocellular afferents work as delay lines, and the laminaris neurons work as co-incidence detectors. The orderly distribution of conduction times, the predictability of favorable interaural time differences from monaural phase responses, and the pattern of the anatomical projection from the nucleus laminaris to the central nucleus of the inferior colliculus suggest that interaural time differences and their phase equivalents are mapped in each frequency band along the dorsoventral axis of the nucleus laminaris.

Interaural time sensitivity in the inferior colliculus of the albino cat

Anatomical studies of the Creel albino cat have demonstrated a pronounced atrophy of cells in the medial superior olive, a structure thought to be important for the detection of interaural time differences (ITDs). We looked for physiological abnormalities in the binaural interaction of cells in three albino cats by recording from single cells in the central nucleus of the inferior colliculus to ITDs of tones and noise. We found that the sensitivity to ITDs of tones and noise was somewhat diminished in the albino cats as compared to normally pigmented cats, though this deficit was only evident when a population of cells was examined. The range of sensitivity of individual cells for both tones and noise was the same in albinos and pigmented animals. Our anatomical measurements showed a smaller reduction in cross-sectional area of cells in the medial superior olive than that reported earlier, and the cell bodies in the medial superior olive of the albinos were less elongated than in normal cats.

Detection of interaural time differences for clicks and tone pips: effects of interaural signal disparity.

The ability to detect small interaural time differences (delta t) was determined in 4 subjects using clicks or long tone pips of various interaural signal disparities which are expressed as the extent of interaural spectral overlaps. The interaural signal disparity was varied by changing (a) the interaural pulse duration difference (delta d) for clicks, or (b) the interaural carrier frequency difference (delta f) for tone pips. In either case, the sensitivity to delta t was maximal under diotic presentations and declined with delta d or delta f. The overall sensitivity to delta t was remarkably higher for clicks than for long tone pips. The results indicate that both (a) the extent of binaural spectral overlaps and (b) the structure of acoustic stimuli are important in detecting small interaural time differences of binaural sounds.

Lateralization of complex waveforms: effects of fine structure, amplitude, and duration.

In recent years there has been an increased interest in the use of interaural time as a cue for lateralization at high frequencies. Our study examines this question using AM complexes with carriers of 1800, 2400, 3000, 3600, 3900, 4200, and 4500 Hz, modulated at 300 Hz and interaurally delayed. The findings indicate that (a) the ability to lateralize these stimuli does not depend on low-frequency distortion, since this ability remains despite the presence of intense low-frequency masking; (b) the task is easier when the entire waveform, rather than just the modulation envelope, is delayed, though this difference seems to decline with practice; (c) the effects of stimulus amplitude and duration on the detection of interaural time differences are reminiscent of those observed with pure tones, although ongoing time differences may be more fully utilized with AM signals; and (d) lateralization declines with interaural carrier frequency discrepancy. We were unable to obtain lateralization of AM complexes at one ear against pure tones (at the modulation frequency) at the other. This strengthens the argument that all stimulus information used is carried in high-frequency channels. Subject Classification: [43]65.62.

Detection of Interaural Time Differences in Short-Duration Low-Frequency Tones

The detectability of interaural time differences (Δt) was investigated as a function of stimulus duration, level, and frequency. Temporally dichotic tone bursts of 250, 500, and 1000 Hz were presented in a two-interval forced choice, in such a way that the signal to one ear led by Δt μsec during either the first or second interval. The tone bursts were 10, 25, 50, 100, and 205 msec in duration and were gated with a rise-decay time of 2.5 msec. The levels used were 50 and 70 dB SPL. Threshold values of Δt were maximal for the shortest durations, then fell rapidly to asymptote in the region from 50 to 100 msec. In addition, thresholds decreased at higher frequencies. Finally, all conditions showed lower thresholds for 70 dB than for 50 dB. The data are fit by a model that treats increased duration as an increase in the number of samples of the interaural difference and describes the improvements found with higher frequencies and levels as a result of the steeper slopes of the displacement waveforms.

Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization.

Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization.