Monaural Pathways Research Articles

Binaural masking-patterns with short signals

In masking-pattern experiments, thresholds are commonly measured for a sinusoidal signal masked by a narrow-band noise as a function of the signal frequency. For a given spectral separation of signal and masker, beating between signal and masker may provide temporal fluctuation cues in addition to energy cues to detect the signal. In a dichotic condition, significantly broader masking patterns were found. It was hypothesized that this is due to the fact that the modulation cues do not play a major role in binaural processing. The present study investigates how masking patterns depend on signal duration. Masking patterns were not only measured for long (600 ms) signals but also for short signals (12 ms), where modulation cues should hardly play a role in signal detection even for monaural detection. The results show broader masking patterns for short signals than for long signals. In addition the binaural benefit does not change as much for the short signals than for the long signals when the signal frequency is varied. A binaural equalization cancellation model predicts the duration dependence of the masking patterns when a modulation analysis is assumed for the monaural pathway only.

The Interaural Time Difference Pathway: a Comparison of Spectral Bandwidth and Correlation Sensitivity at Three Anatomical Levels

Temporal differences between the two ears are critical for spatial hearing. They can be described along axes of interaural time difference (ITD) and interaural correlation, and their processing starts in the brainstem with the convergence of monaural pathways which are tuned in frequency and which carry temporal information. In previous studies, we examined the bandwidth (BW) of frequency tuning at two stages: the auditory nerve (AN) and inferior colliculus (IC), and showed that BW depends on characteristic frequency (CF) but that there is no difference in the mean BW of these two structures when measured in a binaural, temporal framework. This suggested that there is little frequency convergence in the ITD pathway between AN and IC and that frequency selectivity determined by the cochlear filter is preserved up to the IC. Unexpectedly, we found that AN and IC neurons can be similar in CF and BW, yet responses to changes in interaural correlation in the IC were different than expected from coincidence patterns ("pseudo-binaural" responses) in the AN. To better understand this, we here examine the responses of bushy cells, which provide monaural inputs to binaural neurons. Using broadband noise, we measured BW and correlation sensitivity in the cat trapezoid body (TB), which contains the axons of bushy cells. This allowed us to compare these two metrics at three stages in the ITD pathway. We found that BWs in the TB are similar to those in the AN and IC. However, TB neurons were found to be more sensitive to changes in stimulus correlation than AN or IC neurons. This is consistent with findings that show that TB fibers are more temporally precise than AN fibers, but is surprising because it suggests that the temporal information available monaurally is not fully exploited binaurally.

Kcna1Gene Deletion Lowers the Behavioral Sensitivity of Mice to Small Changes in Sound Location and Increases Asynchronous Brainstem Auditory Evoked Potentials But Does Not Affect Hearing Thresholds

Sound localization along the azimuth depends on the sensitivity of binaural nuclei in the auditory brainstem to small differences in interaural level and timing occurring within a submillisecond epoch and on monaural pathways that transmit level and timing cues with high temporal fidelity to insure their coincident arrival at the binaural targets. The soma and axons of these brainstem neurons are heavily invested with ion channels containing the low-threshold potassium channel subunit Kv1.1, which previous in vitro and in vivo studies suggest are important for regulating their high input-output correspondence and temporal synchrony. We compared awake Kcna1-null mutant (Kcna1-/-) mice lacking Kv1.1 with Kcna1+/+ mice to determine whether Kv1.1 activity contributes to sound localization and examined anesthetized mice for absolute hearing thresholds for suprathreshold differences that may be revealed in the waveforms of auditory brainstem response potentials. The awake -/- mice tested with reflex modification audiometry had reduced sensitivity to an abrupt change in the location of a broad band noise compared to +/+ mice, while anesthetized -/- mice had normal absolute thresholds for tone pips but a high level of stimulus-evoked but asynchronous background activity. Evoked potential waveforms had progressively earlier peaks and troughs in -/- mice, but the amplitude excursions between adjacent features were identical in the two groups. Their greater excitability and asynchrony in suprathreshold evoked potentials coupled with their normal thresholds suggests that a disruption in central neural processing in -/- mice and not peripheral hearing loss is responsible for their poor sound localization.

Physiology of the interaction between intensity and time at monaural and binaural stages.

The two cues for azimuthal sound localization, interaural level differences (ILDs) and interaural time differences (ITDs), interact perceptually. According to the latency hypothesis, this interaction arises peripherally: Increases in intensity for the ear nearest to a sound source cause a decrease in response latency relative to the other ear. ILDs would thus shift the pattern of activation in an array of coincidence detectors that processes ITDs. Psychophysical studies have accumulated evidence against the latency hypothesis, but it has received support in several physiological studies that studied transient responses in a variety of binaural structures. We examined the basic premise of peripheral time-intensity trading in the auditory nerve with a coincidence analysis of responses to broadband noise. We found that changes in intensity cause small but systematic shifts in the ongoing timing of responses, generally but not always resulting in shorter delays between stimulus onset and neural response for increasing intensity. Overall, the results show that ongoing timing is remarkably invariant with intensity at the most peripheral neural level. The implication of temporal coding in monaural pathways for binaural ILD processing will be discussed in a wider context. [Supported by the Fund for Scientific Research—Flanders and Research Fund K.U. Leuven.]

Projections from auditory cortex contact cells in the cochlear nucleus that project to the inferior colliculus

Anterograde and retrograde tracing techniques were combined to determine whether auditory cortical axons contact cells in the cochlear nucleus that project to the inferior colliculus. FluoroRuby or fluorescein dextran was injected into auditory cortex to label cortical axons by anterograde transport. Different fluorescent tracers (Fast Blue, FluoroGold, FluoroRuby or fluorescein dextran) were injected into one or both inferior colliculi to label cells in the cochlear nucleus. After 12–15 days, the brain was processed for fluorescence microscopy and the cochlear nuclei were examined for apparent contacts between cortical axons and retrogradely labeled cochlear nucleus cells. The results suggest that axons from the ipsilateral or contralateral cortex contact fusiform and giant cells in the dorsal cochlear nucleus and multipolar cells in the ventral cochlear nucleus that project directly to the inferior colliculus. The contacts occur on cell bodies and dendrites. The target cells in the cochlear nucleus include cells that project ipsilaterally, contralaterally or bilaterally to the inferior colliculus. The results suggest that auditory cortex is in a position to exert direct effects on the monaural pathways that ascend from the cochlear nucleus.

Spike-Frequency Adaptation in the Inferior Colliculus

We investigated spike-frequency adaptation of neurons sensitive to interaural phase disparities (IPDs) in the inferior colliculus (IC) of urethane-anesthetized guinea pigs using a stimulus paradigm designed to exclude the influence of adaptation below the level of binaural integration. The IPD-step stimulus consists of a binaural 3,000-ms tone, in which the first 1,000 ms is held at a neuron's least favorable ("worst") IPD, adapting out monaural components, before being stepped rapidly to a neuron's most favorable ("best") IPD for 300 ms. After some variable interval (1-1,000 ms), IPD is again stepped to the best IPD for 300 ms, before being returned to a neuron's worst IPD for the remainder of the stimulus. Exponential decay functions fitted to the response to best-IPD steps revealed an average adaptation time constant of 52.9 +/- 26.4 ms. Recovery from adaptation to best IPD steps showed an average time constant of 225.5 +/- 210.2 ms. Recovery time constants were not correlated with adaptation time constants. During the recovery period, adaptation to a 2nd best-IPD step followed similar kinetics to adaptation during the 1st best-IPD step. The mean adaptation time constant at stimulus onset (at worst IPD) was 34.8 +/- 19.7 ms, similar to the 38.4 +/- 22.1 ms recorded to contralateral stimulation alone. Individual time constants after stimulus onset were correlated with each other but not with time constants during the best-IPD step. We conclude that such binaurally derived measures of adaptation reflect processes that occur above the level of exclusively monaural pathways, and subsequent to the site of primary binaural interaction.

The role of spectral change detectors in temporal order judgment of tones.

Human listeners can judge the temporal order of acoustic events quite accurately in certain conditions. We hypothesized that this accuracy is realized by coding temporal order as a single neural code of spectral change in the auditory system. To test this hypothesis, we examined whether adaptation to linear frequency glides affects subsequent temporal order judgment of brief tones. We found that the point of subjective simultaneity between two tones shifted depending on the direction of spectral change of the adaptor, as predicted by the hypothesis. The amount of aftereffect was significantly reduced when adaptor and test tones were presented in different frequency regions or to different ears, suggesting that the relevant neural units exist predominantly in a frequency-selective monaural pathway.

Measurements of precedence phenomena in binaural and monaural conditions

The precedence effect is a compelling auditory illusion which is thought to negotiate competition for perception and localization between the direct sound and its reflections. Three perceptual phenomena that have been related to the precedence effect are known to occur: (1) the two sounds are fused into one auditory event (fusion); (2) the perceived location of the fused auditory event is dominated by the leading source (localization dominance); and (3) directional information from the lagging source is inaccessible (discrimination suppression). Performance was measured on the above tasks under both binaural and monaural conditions, in both the azimuthal and median-sagittal planes, and in listeners with profound monaural deafness. Results suggest that: (1) Fusion occurs at similar delays under monaural and binaural conditions; (2) discrimination suppression is strong under binaural conditions but weak or absent under monaural conditions; (3) localization dominance is similar in the azimuthal and median-sagittal planes. It is tentatively concluded that the precedence effect may not be mediated solely by binaural circuits, but that monaural pathways may be involved as well. [Work supported by NIH Grant Nos. DC02692 and DC00100.]

Time discrimination and amplitude modulation (AM) detection

The model [N. Todd, ‘‘A theory of the principal monaural pathway I. Pitch and time perception,’’ J. Acoust. Soc. Am. 99, 2491(A) (1996)] proposes also to account for the psychophysics of time by the interaction of a ‘‘sensory memory,’’ in the form of the collective response of cortical bandpass cells, and a ‘‘long-term memory,’’ which is the result of learning in a cortical neural network. Since the time constants of the cortical cells are relatively long, their response to an inferior collicular (ICC) input lasts long after the ICC input has ceased (and hence the form of the sensory memory above). The cortical amplitude modulation response is roughly a Laplace transform of the ICC response envelope, and so is highly dependent on envelope duration. The cortical response thus captures both the pitch and durational properties of the tone. It is shown how this model is able to provide an account of two fundamental aspects of auditory temporal processing: (1) the psychophysical law for time interval discrimination and (2) the psychophysical law for AM detection. The model is further applied to the problem of the ‘‘filled interval illusion,’’ which hitherto has evaded a convincing explanation.

A theory of the principal monaural pathway. I. Pitch and time perception.

A theory of the principal monaural pathway is described according to which temporal information is spatially coded on three dimensions roughly corresponding to the levels of, respectively, the cochlea, the inferior colliculus, and the auditory cortex [C. Schreiner and G. Langner, ‘‘Coding of temporal patterns in the central auditory nervous system,’’ Auditory Function: Neurobiological Bases of Hearing, edited by G. M. Edelman et al. (Wiley, New York, 1988), pp. 337–361]. This theory is expressed in the form of a computational model which simulates peripheral and central processing and which has the following main components: (1) a one‐dimensional linear bandpass filter‐bank to simulate the cochlea; (2) a two‐dimensional amplitude‐modulation (AM) bandpass filter‐bank to simulate the colliculus; (3) a three‐dimensional AM bandpass filter‐bank to simulate layer IV receptive cells in the cortex; (4) a cortical cross‐channel correlation mechanism; and (5) a central pattern recognition mechanism. Overall, periodicity pitch (i.e., periods of up to about 1000 Hz) is primarily associated with subcortical processing whereas time and rhythm (i.e., periods of up to about 20 Hz) are primarily associated with cortical processing. The model is applied to the following phenomena: virtual pitch shift, musical chords, the psychophysical law for interval discrimination, and the filled interval illusion.

A theory of the principal monaural pathway. II. Rhythm, streaming, and comodulation masking release.

The model [N. Todd, ‘‘A theory of the principal monaural pathway. I. Pitch and time perception,’’ J. Acoust. Soc. Am. (these proceedings)] proposes to account for auditory streaming by a cross‐correlation mechanism modeled as an array of cortical columns. A column contains excilatory and inhibitory interneurons and pyramidal cells which receive input from both the thalamus and from neighboring columns. For columns with coherent thalamic inputs, the outputs of the pyramids sum across frequency because local interneurons compute a correlation between the AM transform of the inputs of the local and remote columns, and selectively gate the input to the pyramidal cell. (1) Grouping by frequency proximity—for columns separated by less than a critical band, thalamic inputs are unresolved. (2) Grouping by temporal proximity—at repetition rates below the mean of the AM distribution, AM fundamentals are less well represented; at higher repetition rates the AM harmonics are more separated. (3) Temporal development—where the AM spectra take time to develop. The AM coherence mechanism also gates the inputs to disjoint subpopulations of a low‐pass mechanism, and thus also accounts for comodulation masking release, since backward masking will only take place within a single subpopulation.

Convergence and divergence of ascending binaural and monaural pathways from the superior olives of the mustached bat

The lateral superior olive and medial superior olive give rise to pathways that terminate in the dorsal nucleus of the lateral lemniscus and central nucleus of the inferior colliculus. In most mammals, neurons in both the medial and lateral superior olives are binaural, but in the mustached bat most neurons in the medial superior olive are monaural. The aims of this study were to determine how the inputs to the medial superior olive contribute to its monaurality and to determine whether the ascending projections from the lateral and medial superior olives overlap or remain segregated at their targets. Injections of two different tracers were placed in tonotopically matched areas of the lateral and medial superior olives in the same animal. Retrograde transport from injections in the medial superior olive labeled spherical cells in the contralateral anteroventral cochlear nucleus and principal cells in the ipsilateral medial nucleus of the trapezoid body. Few cells were labeled in ipsilateral cochlear nucleus. Anterograde transport resulted in tonotopically specific distributions of label with the same laterality as in nonecholocating mammals. In the dorsal nucleus of the lateral lemniscus, label from the lateral and medial superior olives largely overlapped. In the inferior colliculus, label from the lateral and medial superior olives largely overlapped. In the inferior colliculus, label from the two sources overlapped in the high and low frequency ranges, but in the frequency range around 60 kHz, label from the medial superior olive extended more dorsally than that from the lateral superior olive. These results indicate that projections of the lateral and medial superior olives overlap extensively at their targets.

Brain stem mechanisms for sound localization: Monaural and binaural pathways to the inferior colliculus

The current view that the medial and lateral superior olives have binaural functions related to localization of sound in space grew, in part, from observations on the ascending connections to these nuclei. The anteroventral cochlear nucleus is the origin of the major projections to these nuclei, which in turn, project as a “binaural pathway” to the inferior colliculus. Because the anteroventral cochlear nucleus is also the source of a “monaural pathway” to the contralateral inferior colliculus, the question arises as to whether or not these two pathways overlap at the inferior colliculus. Our anatomical evidence shows that these two pathways converge in the lateral part of the central nucleus of the inferior colliculus of the tree shrew. Observations on these pathways in other mammals suggest that this convergence is a general feature in mammalian auditory pathways. Behavioral evidence suggests that both binaural and monaural pathways are important for localization of sound in space. [Supported by grants from NIH and NSF.]