Daniel J. Tollin

The Lateral Superior Olive: A Functional Role in Sound Source Localization

Sound location in azimuth is signaled by differences in the times of arrival (interaural time difference, ITDs) and the amplitudes (interaural level differences, ILDs) of the stimuli at the ears. Psychophysical studies have shown that low- and high-frequency sounds are localized based on ITDs and ILDs, respectively, suggesting that dual mechanisms mediate localization. The anatomical and physiological bases for this “duplex theory” of localization are found in the medial (MSO) and lateral (LSO) superior olives, two of the most peripheral sites in the ascending auditory pathway receiving inputs from both ears. The MSO and LSO are believed to be responsible for the initial encoding of ITDs and ILDs, respectively. Here the author focuses on ILDs as a cue to location and the role of the LSO in encoding ILDs. Evidence from disparate fields of study supports the hypothesis that the LSO is the initial ILD processor in the mammalian auditory system. NEUROSCIENTIST 9(2): 127–143, 2003.

Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive.

The lateral superior olive (LSO) is believed to encode differences in sound level at the two ears, a cue for azimuthal sound location. Most high-frequency-sensitive LSO neurons are binaural, receiving inputs from both ears. An inhibitory input from the contralateral ear, via the medial nucleus of the trapezoid body (MNTB), and excitatory input from the ipsilateral ear enable level differences to be encoded. However, the classical descriptions of low-frequency-sensitive neurons report primarily monaural cells with no contralateral inhibition. Anatomical and physiological evidence, however, shows that low-frequency LSO neurons receive low-frequency inhibitory input from ipsilateral MNTB, which in turn receives excitatory input from the contralateral cochlear nucleus and low-frequency excitatory input from the ipsilateral cochlear nucleus. Therefore, these neurons would be expected to be binaural with contralateral inhibition. Here, we re-examined binaural interaction in low-frequency (less than ∼3 kHz) LSO neurons and phase locking in the MNTB. Phase locking to low-frequency tones in MNTB and ipsilaterally driven LSO neurons with frequency sensitivities <1.2 kHz was enhanced relative to the auditory nerve. Moreover, most low-frequency LSO neurons exhibited contralateral inhibition: ipsilaterally driven responses were suppressed by raising the level of the contralateral stimulus; most neurons were sensitive to interaural time delays in pure tone and noise stimuli such that inhibition was nearly maximal when the stimuli were presented to the ears in-phase. The data demonstrate that low-frequency LSO neurons of cat are not monaural and can exhibit contralateral inhibition like their high-frequency counterparts.

The acoustical cues to sound location in the rat: Measurements of directional transfer functions

The acoustical cues for sound location are generated by spatial- and frequency-dependent filtering of propagating sound waves by the head and external ears. Although rats have been a common model system for anatomy, physiology, and psychophysics of localization, there have been few studies of the acoustical cues available to rats. Here, directional transfer functions (DTFs), the directional components of the head-related transfer functions, were measured in six adult rats. The cues to location were computed from the DTFs. In the frontal hemisphere, spectral notches were present for frequencies from approximately 16 to 30 kHz; in general, the frequency corresponding to the notch increased with increases in source elevation and in azimuth toward the ipsilateral ear. The maximum high-frequency envelope-based interaural time differences (ITDs) were 130 mus, whereas low-frequency (<3.5 kHz) fine-structure ITDs were 160 mus; both types of ITDs were larger than predicted from spherical head models. Interaural level differences (ILDs) strongly depended on location and frequency. Maximum ILDs were <10 dB for frequencies <8 kHz and were as large as 20-40 dB for frequencies >20 kHz. Removal of the pinna eliminated the spectral notches, reduced the acoustic gain and ILDs, altered the acoustical axis, and reduced the ITDs.

Round Window Membrane Implantation with an Active Middle Ear Implant: A Study of the Effects on the Performance of Round Window Exposure and Transducer Tip Diameter in Human Cadaveric Temporal Bones

Objectives: To assess the importance of 2 variables, transducer tip diameter and resection of the round window (RW) niche, affecting the optimization of the mechanical stimulation of the RW membrane with an active middle ear implant (AMEI). Materials and Methods: Ten temporal bones were prepared with combined atticotomy and facial recess approach to expose the RW. An AMEI stimulated the RW with 2 ball tip diameters (0.5 and 1.0 mm) before and after the resection of the bony rim of the RW niche. The RW drive performance, assessed by stapes velocities using laser Doppler velocimetry, was analyzed in 3 frequency ranges: low (0.25–1 kHz), medium (1–3 kHz) and high (3–8 kHz). Results: Driving the RW produced mean peak stapes velocities (HEV) of 0.305 and 0.255 mm/s/V at 3.03 kHz, respectively, for the 1- and 0.5-mm tips, with the RW niche intact. Niche drilling increased the HEV to 0.73 and 0.832 mm/s/V for the 1- and 0.5-mm tips, respectively. The tip diameter produced no difference in output at low and medium frequencies; however, the 0.5-mm tip was 5 and 6 dB better than the 1-mm tip at high frequencies before and after niche drilling, respectively. Drilling the niche significantly improved the output by 4 dB at high frequencies for the 1-mm tip, and by 6 and 10 dB in the medium- and high-frequency ranges for the 0.5-mm tip. Conclusion: The AMEI was able to successfully drive the RW membrane in cadaveric temporal bones using a classical facial recess approach. Stimulation of the RW membrane with an AMEI without drilling the niche is sufficient for successful hearing outputs. However, the resection of the bony rim of the RW niche significantly improved the RW stimulation at medium and higher frequencies. Drilling the niche enhances the exposure of the RW membrane and facilitates positioning the implant tip.

Postnatal development of sound pressure transformations by the head and pinnae of the cat: monaural characteristics.

Although there have been many anatomical, physiological, and psychophysical studies of auditory development in cat, there have been no comparable studies of the development of the sound pressured transformations by the cat head and pinnae. Because the physical dimensions of the head and pinnae determine the spectral and temporal transformations of sound, as head and pinnae size increase during development, the magnitude and frequency ranges of these transformations are hypothesized to systematically change. This hypothesis was tested by measuring directional transfer functions (DTFs), the directional components of head-related transfer functions, and the linear dimensions of the head and pinnae in cats from the onset of hearing ( approximately 1.5 weeks) through adulthood. Head and pinnae dimensions increased by factors of approximately 2 and approximately 2.5, respectively, reaching adult values by approximately 23 and approximately 16 weeks, respectively. The development of the spectral notch cues to source location, the spatial- and frequency-dependent distributions of DTF amplitude gain (acoustic directionality), maximum gain, and the acoustic axis, and the resonance frequency and associated gain of the ear canal and concha were systematically related to the dimensions of the head and pinnae. These monaural acoustical properties of the head and pinnae in the cat are mature by 16 weeks.

Interaural Level Difference Discrimination Thresholds for Single Neurons in the Lateral Superior Olive

The lateral superior olive (LSO) is one of the earliest sites in the auditory pathway that is involved in processing acoustical cues to sound location. Here, we tested the hypothesis that LSO neurons can signal small changes in interaural level differences (ILDs), a cue to horizontal sound location, of pure tones based on discharge rate consistent with psychophysical performance in the discrimination of ILDs. Neural thresholds for ILD discrimination were determined from the discharge rates and associated response variability of single units in response to 300 ms tones in the LSO of barbiturate-anesthetized cats using detection theory. Neural response variability was well described by a power function of the mean rate, both in individual neurons and collectively; LSO neurons were less variable than expected from a Poisson process. Compared with psychophysical data, the best-threshold ILDs of single LSO neurons were comparable with or better than behavior over the full range of frequencies (0.3–35 kHz) and pedestal ILDs (±25 dB) explored in this study. With a pedestal ILD of 0 dB, ILD increments of 1 dB could be discriminated by some neurons, with a median of 4.35 dB across neurons. For pedestal ILDs away from 0 dB, the best-threshold ILDs were as low as 0.5 dB, with a median of 2.3 dB. These findings support the hypothesis that the LSO plays a role in the extraction of ILD, and that the representation of ILD by LSO neurons may set a lower bound on the behavioral sensitivity to ILDs.

Toward a Mouse Neuroethology in the Laboratory Environment

In this report we demonstrate that differences in cage type brought unexpected effects on aggressive behavior and neuroanatomical features of the mouse olfactory bulb. A careful characterization of two cage types, including a comparison of the auditory and temperature environments, coupled with a demonstration that naris occlusion abolishes the neuroanatomical changes, lead us to conclude that a likely important factor mediating the phenotypic changes we find is the olfactory environment of the two cages. We infer that seemingly innocuous changes in cage environment can affect sensory input relevant to mice and elicit profound effects on neural output. Study of the neural mechanisms underlying animal behavior in the laboratory environment should be broadened to include neuroethological approaches to examine how the laboratory environment (beyond animal well-being and enrichment) influences neural systems and behavior.

Varying Overall Sound Intensity to the Two Ears Impacts Interaural Level Difference Discrimination Thresholds by Single Neurons in the Lateral Superior Olive

The lateral superior olive (LSO) is one of the earliest sites in the auditory pathway involved in processing acoustical cues to sound location. LSO neurons encode the interaural level difference (ILD) cue to azimuthal location. Here we investigated the effect of variations in the overall stimulus levels of sounds at the two ears on the sensitivity of LSO neurons to small differences in ILDs of pure tones. The neuronal firing rate versus ILD functions were found to depend greatly on the overall stimulus level, typically shifting along the ILD axis toward the excitatory ear and attaining greater maximal firing rates as stimulus level increased. Seventy-five percent of neurons showed significant shifts with changes in overall sound level. The range of ILDs corresponding to best neural acuity for ILDs shifted accordingly. In a simulation using the empirical data, when the overall stimulus level was randomly changed from one trial to the next, the neural discrimination thresholds for ILD, or ILD acuities, were worsened by 50-60% across the population of neurons relative to fixed stimulus levels whether ILD acuity was measured at the azimuthal midline or the ILD pedestal producing the best acuity. The impairment in ILD discrimination was attributed to the increased neural response variance imparted by varying the stimulus level. These results contrast to those observed in psychophysical studies where ILD discrimination thresholds under similar experimental conditions are invariant to overall changes in stimulus level. A simple computational model that incorporated the antagonistic inputs of bilateral LSO nuclei as well as the dorsal nuclei of the lateral lemniscus to the inferior colliculus produced a more robust encoding of ILD even in the setting of roving stimulus level. Testable predictions of this model and comparison to other computational models addressing stimulus invariance were considered.

The precedence effect in sound localization.

In ordinary listening environments, acoustic signals reaching the ears directly from real sound sources are followed after a few milliseconds by early reflections arriving from nearby surfaces. Early reflections are spectrotemporally similar to their source signals but commonly carry spatial acoustic cues unrelated to the source location. Humans and many other animals, including nonmammalian and even invertebrate animals, are nonetheless able to effectively localize sound sources in such environments, even in the absence of disambiguating visual cues. Robust source localization despite concurrent or nearly concurrent spurious spatial acoustic information is commonly attributed to an assortment of perceptual phenomena collectively termed “the precedence effect,” characterizing the perceptual dominance of spatial information carried by the first-arriving signal. Here, we highlight recent progress and changes in the understanding of the precedence effect and related phenomena.

Electrocochleographic and mechanical assessment of round window stimulation with an active middle ear prosthesis.

Mechanical stimulation of the round window (RW) with an active middle ear prosthesis (AMEP) has shown functional benefit in clinical reports in patients with mixed hearing loss (MHL). Further objective physiological data on the efficacy of RW stimulation is needed, however, to demonstrate that RW stimulation with an AMEP can generate input to the inner ear comparable to acoustic input. Cochlear microphonic (CM) and mechanical (stapes velocity) responses to sinusoidal stimuli were measured by electrode and laser Doppler vibrometry in eight chinchillas in response to normal acoustic stimulation via sealed calibrated insert earphones and to AMEP stimulation (Otologics MET, Boulder, CO, USA) of the RW with and without lateral ossicular chain disarticulation. CM thresholds for acoustic stimulation were frequency dependent and ranged from 16 to 50 dB SPL. CM thresholds measured with RW stimulation ranged from -14 to 35 dBmV with an intact middle ear chain and from -7 to 36 dBmV after lateral ossicular chain disarticulation. Acoustically, stapes velocity maxima was observed at approximately 700 Hz and minima at approximately 2.65 kHz. With application of the AMEP to the RW, peak stapes velocity was observed at 2-3 kHz. The equivalent ear canal sound pressure level (L(E)(max)dB SPL) evoked by RW stimulation with the AMEP was 60-105 dB SPL for the intact middle ear and 70-100 dB SPL after ossicular chain disarticulation. Stimulating the inner ear through the RW with an AMEP produces evoked responses (CM) comparable to normal acoustic input. When adjusted for threshold (due to unit differences, dB SPL or dB mV), the sensitivity of the CM (slope) for acoustic was comparable to sensitivities obtained by AMEP stimulation of the RW. Mechanical stimulation of the RW with an AMEP produces cochlear responses (CMs) and stapes velocities that are functionally equivalent to acoustic stimulation.