Tom C. T. Yin

Coincidence Detection in the Auditory System: 50 Years after Jeffress

The result of Jeffress’ model is a representation of ITD as a spatial activity profile in an array of tuned cells. Unfortunately, this part of the model has been the most elusive to document. Best ITDs in the MSO are strongly biased toward the contralateral hemifield and fall mostly within the range of ITDs naturally encountered by a cat (0–400 μs) (Yin and Chan 1990xYin, T.C.T. and Chan, J.C.K. J. Neurophysiol. 1990; 64: 465–488PubMedSee all ReferencesYin and Chan 1990). Moreover, there is a significant correlation between the best ITDs and the rostrocaudal location of recording sites pooled from different experiments. The most rostrally located cells prefer small ITDs, while cells located caudally prefer large positive ITDs as generated by sounds in the contralateral hemifield (Figure 1CFigure 1C). However, the relationship is quite scattered and needs to be reexamined by methods that do not necessitate pooling across animals. Importantly, it is in agreement with the anatomical findings on contralateral delay lines extending rostral to caudal, which predict best ITDs to be small rostrally and large caudally. This observation departs from the original scheme of Jeffress, in which ITDs corresponding to both ipsi- and contralaterally located sources are encoded on both sides of the brain, but it is consonant with the contralateralization generally found in other sensory and motor systems.In conclusion, the current view on binaural time processing contains the essential features proposed by Jeffress. Just as Hubel and Wiesel’s model of orientation selectivity has provided a bull’s eye for vision research, the simple model introduced by Jeffress has served as a focal point in audition and has sparked many computational and experimental studies, illustrating the heuristic value of such qualitative models in neuroscience. To end, we mention one particularly interesting study that bridges the gap between human psychophysics and experimental studies in animals. Multiple sclerosis patients with focal lesions in the pons showed abnormal discrimination of ITDs, as well as abnormalities in their brainstem evoked responses, but could still discriminate interaural intensity differences (Levine et al. 1993xLevine, R.A., Gardner, J.C., Stufflebeam, S.M., Fullerton, B.C., Carlisle, E.W., Furst, M., Rosen, B.R., and Kiang, N.Y.S. Hear. Res. 1993; 68: 59–72Crossref | PubMed | Scopus (28)See all ReferencesLevine et al. 1993). These findings were interpretable in the framework of Jeffress’ model by assuming that demyelination caused a desynchronization or decorrelation of the spike patterns fed to the binaural processor. Such decorrelation impairs discrimination of ITDs but not of intensity differences, which are usually thought to require a comparison of average spike counts and to be unaffected by disruption of fine time structure. While this study does not bear directly on the details of the Jeffress model, it provides a compelling argument for the importance of spike timing in human auditory functioning.§To whom correspondence should be addressed (e-mail: yin@physiology.wisc.edu).

A matter of time: internal delays in binaural processing.

As an animal navigates its surroundings, the sounds reaching its two ears change in waveform similarity (interaural correlation) and in time of arrival (interaural time difference, ITD). Humans are exquisitely sensitive to these binaural cues, and it is generally agreed that this sensitivity involves coincidence detectors and internal delays that compensate for external acoustic delays (ITDs). Recent data show an unexpected relationship between the tuning of a neuron to frequency and to ITD, leading to several proposals for sources of internal delay and the neural coding of interaural temporal cues. We review the alternatives, and argue that an understanding of binaural mechanisms requires consideration of sensitivity not only to ITDs, but also to interaural correlation.

Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat

The inferior colliculus (IC) is a major auditory structure that integrates synaptic inputs from ascending, descending, and intrinsic sources. Intracellular recording in situ allows direct examination of synaptic inputs to the IC in response to acoustic stimulation. Using this technique and monaural or binaural stimulation, responses in the IC that reflect input from a lower center can be distinguished from responses that reflect synaptic integration within the IC. Our results indicate that many IC neurons receive synaptic inputs from multiple sources. Few, if any, IC neurons acted as simple relay cells. Responses often displayed complex interactions between excitatory and inhibitory sources, such that different synaptic mechanisms could underlie similar response patterns. Thus, it may be an oversimplification to classify the responses of IC neurons as simply excitatory or inhibitory, as is done in many studies. In addition, inhibition and intrinsic membrane properties appeared to play key roles in creating de novo temporal response patterns in the IC.

Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat

The precedence effect (PE) describes an illusion produced when two similar sounds are delivered in quick succession (interclick delays of 2–8 msec) from sound sources at different locations so that only a single sound is perceived. The localization of the perceived sound is dominated by the location of the leading sound. If the delays are very short (< 1–2 msec), summing localization occurs and a phantom source is perceived whose location is toward the leading sound. The purpose of these experiments was to look for physiological correlates of the precedence effect and summing localization by recording from single neurons in the inferior colliculus of the anesthetized cat. Click stimuli were delivered under two different situations: over headphones in dichotic experiments and through two speakers in an anechoic room in free-field studies. In the latter case the cat was placed midway between the speakers and a single click stimulus was delivered to each speaker with variable interclick delays (ICDs). Most cells, under both dichotic and free-field conditions, exhibited a form of the precedence effect in which the response to the lagging click was suppressed when ICDs were short. The suppression of the lagging click, or echo, was measured by recovery curves, which plotted the response of the lagging click as a function of ICD. There was considerable variability in the recovery curves from different cells: the ICDs at which the recovery reached 50%, which is a measure of the echo threshold for the cell, ranged from 1 to 100 msec with a median of 20 msec. Human psychophysical experiments report echo thresholds for clicks ranging from 2 to 8 msec. If we assume that absolute echo threshold is determined by the cells with shortest recovery curves, then the thresholds for single cells are in accord with the psychophysical results. The possible sites of generation of the echo suppression are also considered. Changes in the relative level of the leading and lagging clicks produced the expected shifts in the recovery curves. With short ICDs in the summing localization range (between about +/- 2 msec) cells also showed responses consonant with the human psychophysical result that the sound source is localized to a phantom image between the two speakers and toward the leading one. The location of the image varied systematically with the relative levels or ICDs of the clicks.(ABSTRACT TRUNCATED AT 250 WORDS)

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.

Behavioral Studies of Sound Localization in the Cat

Using the magnetic search coil technique to measure eye and ear movements, we trained cats by operant conditioning to look in the direction of light and sound sources with their heads fixed. Cats were able to localize noise bursts, single clicks, or click trains presented from sources located on the horizontal and vertical meridians within their oculomotor range. Saccades to auditory targets were less accurate and more variable than saccades to visual targets at the same spatial positions. Localization accuracy of single clicks was diminished compared with the long-duration stimuli presented from the same sources. Control experiments with novel auditory targets, never associated with visual targets, demonstrated that the cats localized the sound sources using acoustic cues and not from memory. The role of spectral features imposed by the pinna for vertical sound localization was shown by the breakdown in localization of narrow-band (one-sixth of an octave) noise bursts presented from sources along the midsagittal plane. In addition, we show that cats experience summing localization, an illusion associated with the precedence effect. Pairs of clicks presented from speakers at (±18°,0°) with interclick delays of ±300 μsec were perceived by the cat as originating from phantom sources extending from the midline to approximately ±10°.

Interaural time sensitivity of high‐frequency neurons in the inferior colliculus

Recent psychoacoustic experiments have shown that interaural time differences provide adequate cues for lateralizing high-frequency sounds, provided the stimuli are complex and not pure tones. We present here physiological evidence in support of these findings. Neurons of high best frequency in the cat inferior colliculus respond to interaural phase differences of amplitude modulated waveforms, and this response depends upon preservation of phase information of the modulating signal. Interaural phase differences were introduced in two ways: by interaural delays of the entire waveform and by binaural beats in which there was an interaural frequency difference in the modulating waveform. Results obtained with these two methods are similar. Our results show that high-frequency cells can respond to interaural time differences of amplitude modulated signals and that they do so by a sensitivity to interaural phase differences of the modulating waveform.

Responses of Cochlear Nucleus Cells and Projections of their Axons

The advent of intracellular recording using horseradish peroxidase-filled glass electrodes offered a new and exciting approach to the in vivo cochlear nucleus (CN) preparation. Sharp glass microelectrodes, filled with a standard salt solution containing positively charged HRP molecules, made it feasible to record and characterize supra- and subthreshold intracellular responses of individual neurons to auditory stimuli, inject and subsequently recover the same HRP-labeled cell and ask the following basic questions; 1) Do morphologically defined cell types in the cochlear nucleus respond in a certain way to simple auditory stimuli at both the sub- and suprathreshold level? 2) Are the synaptic inputs of different cell types different, in terms of location, type and concentration, and are they arranged in ways that might help to explain the cell type’s unique responsiveness? 3) What is the projection pattern of individual axons originating from a given cell type, what are the shapes of vesicles within the terminals of these axons and can we make educated guesses about their influence on other cell populations based on this information?

Physiological Studies of Directional Hearing

This review concerns physiological studies of the neural mechanisms of sound localization. We will describe the responses of neurons in the central auditory system to sounds presented dichotically or in the free field. The free‐field studies have sought to define the spatial receptive fields of these neurons and their topographical organization in the brain. Although the functional aspects of these cells are most effectively addressed by free‐field methods, the mechanism by which these cells accomplish this task is best studied using dichotic stimulation. Influenced by the duplex theory and human psychoacoustics, the major focus of neurophysiological studies using dichotic stimulation has been the investigation of the effects of varying interaural phase and intensity. The neuronal responses to these stimuli and their relationship to the frequency domain will be discussed with a particular emphasis on the concept of characteristic delay. In an attempt to define the underlying circuitry, we will compare the...

Cross Correlation by Neurons of the Medial Superior Olive: a Reexamination

Initial analysis of interaural temporal disparities (ITDs), a cue for sound localization, occurs in the superior olivary complex. The medial superior olive (MSO) receives excitatory input from the left and right cochlear nuclei. Its neurons are believed to be coincidence detectors, discharging when input arrives simultaneously from the two sides. Many current psychophysical models assume a strict version of coincidence, in which neurons of the MSO cross correlate their left and right inputs. However, there have been few tests of this assumption. Here we examine data derived from two earlier studies of the MSO and compare the responses to the output of a computational model. We find that the MSO is not an ideal cross correlator. Ideal cross correlation implies a strict relationship between the precision of phase-locking of the inputs and the range of ITDs to which a neuron responds. This relationship does not appear to be met. Instead, the modeling implies that a neuron responds over a wider range of ITDs than expected from the inferred precision of phase-locking of the inputs. The responses are more consistent with a scheme in which the neuron can also be activated by the input from one side alone. Such activation degrades the tuning of neurons in the MSO to ITDs.