Envelope Coding in the Lateral Superior Olive. III. Comparison With Afferent Pathways

Joris, Philip X. and Tom C. T. Yin. Envelope coding in the lateral superior olive. III. Comparison with afferent pathways. J. Neurophysiol. 79: 253–269, 1998. Binaural cues for spatial localization of complex high-frequency sounds are interaural level and time differences (ILDs and ITDs). We previously showed that cells in the lateral superior olive (LSO) are sensitive to ITDs in the envelope of sinusoidally amplitude-modulated (AM) signals up to a modulation frequency of only ∼800 Hz. To understand the limitations in this ITD-sensitivity, we here compare responses to monaural modulation in LSO and its input pathways, derived from cochlear nucleus and medial nucleus of the trapezoid body. These pathways have marked functional and morphological specializations, suggestive of adaptations for timing. Afferent cell populations were identified on the basis of electrophysiological signatures, and for each population, average firing rate and synchronization to AM tones were compared with auditory-nerve fibers and LSO cells. Except for an increase in modulation gain in some subpopulations, synchronization of LSO afferents was very similar to that in auditory nerve fibers in its dependency on sound pressure level (SPL), modulation depth, and modulation frequency. Distributions of cutoff frequencies of modulation transfer functions were largely coextensive with the distribution in auditory nerve. Group delays, measured from the phase of the response modulation as a function of modulation frequency, showed an orderly dependence on characteristic frequency and cell type and little dependence on SPL. Similar responses were obtained to a modulated broadband carrier. Compared with their afferents, LSO cells synchronized to monaurally modulated stimuli with a higher gain but often over a narrower range of modulation frequencies. Considering the scatter in afferent and LSO cell populations, ipsi- and contralateral responses were well matched in cutoff frequency and magnitude of delays. In contrast to their afferents, LSO cells show a decrease in average firing rate at high modulation frequencies. We conclude that the restricted modulation frequency range over which LSO cells show ITD-sensitivity does not result from loss of envelope information along the afferent pathway but is due to convergence or postsynaptic effects at the level of the LSO. The faithful transmission of envelope phase-locking in LSO afferents is consistent with their physiological and morphological adaptations, but these adaptations are not commensurate with the rather small effects of physiological ITDs reported previously, especially when compared with effects of ILDs. We suggest that these adaptations have evolved to allow a comparison of instantaneous amplitude fluctuations at the two ears rather than to extract interaural timing information per se.

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Encoding timing and intensity in the ventral cochlear nucleus of the cat

Journal of Neurophysiology ◽

10.1152/jn.1986.56.2.261 ◽

1986 ◽

Vol 56 (2) ◽

pp. 261-286 ◽

Cited By ~ 242

Author(s):

W. S. Rhode ◽

P. H. Smith

Keyword(s):

Firing Rate ◽

Cochlear Nucleus ◽

Auditory Nerve ◽

Cell Types ◽

Nerve Fibers ◽

Frequency Selectivity ◽

Firing Rates ◽

Ventral Cochlear Nucleus ◽

Auditory Nerve Fibers ◽

Different Cell Types

Physiological response properties of neurons in the ventral cochlear nucleus have a variety of features that are substantially different from the stereotypical auditory nerve responses that serve as the principal source of activation for these neurons. These emergent features are the result of the varying distribution of auditory nerve inputs on the soma and dendrites of the various cell types within the nucleus; the intrinsic membrane characteristics of the various cell types causing different responses to the same input in different cell types; and secondary excitatory and inhibitory inputs to different cell types. Well-isolated units were recorded with high-impedance glass microelectrodes, both intracellularly and extracellularly. Units were characterized by their temporal response to short tones, rate vs. intensity relation, and response areas. The principal response patterns were onset, chopper, and primary-like. Onset units are characterized by a well-timed first spike in response to tones at the characteristic frequency. For frequencies less than 1 kHz, onset units can entrain to the stimulus frequency with greater precision than their auditory nerve inputs. This implies that onset units receive converging inputs from a number of auditory nerve fibers. Onset units are divided into three subcategories, OC, OL, and OI. OC units have extraordinarily wide dynamic ranges and low-frequency selectivity. Some are capable of sustaining firing rates of 800 spikes/s at high intensities. They have the smallest standard deviation and coefficient of variation of the first spike latency of any cells in the cochlear nuclei. OC units are candidates for encoding intensity. OI and OL units differ from OC units in that they have dynamic ranges and frequency selectivity ranges much like those of auditory nerve fibers. They differ from one another in their steady-state firing rates; OI units fire mainly at the onset of a tone. OI units also differ from OL units in that they prefer frequency sweeps in the low to high direction. Primary-like-with-notch (PLN) units also respond to tones with a well-timed first spike. They differ from onset cells in that the onset peak is not always as precise as the spontaneous rate is higher. A comparison of spontaneous firing rate and saturation firing rate of PLN units with auditory nerve fibers suggest that PLN units receive one to four auditory nerve fiber inputs. Chopper units fire in a sustained regular manner when they are excited by sound.(ABSTRACT TRUNCATED AT 400 WORDS)

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Neural correlates of the pitch of complex tones. II. Pitch shift, pitch ambiguity, phase invariance, pitch circularity, rate pitch, and the dominance region for pitch

Journal of Neurophysiology ◽

10.1152/jn.1996.76.3.1717 ◽

1996 ◽

Vol 76 (3) ◽

pp. 1717-1734 ◽

Cited By ~ 154

Author(s):

P. A. Cariani ◽

B. Delgutte

Keyword(s):

Auditory Nerve ◽

Modulation Frequency ◽

Low Frequency ◽

Neural Correlates ◽

Nerve Fibers ◽

Fundamental Period ◽

Complex Tones ◽

Auditory Nerve Fibers ◽

High Pass ◽

Pitch Shift

1. The neural correlates of low pitches produced by complex tones were studied by analyzing temporal discharge patterns of auditory nerve fibers in Dial-anesthetized cats. In the previous paper it was observed that, for harmonic stimuli, the most frequent interspike interval present in the population of auditory nerve fibers always corresponded to the perceived pitch (predominant interval hypothesis). The fraction of these most frequent intervals relative to the total number of intervals qualitatively corresponded to strength (salience) of the low pitches that are heard. 2. This paper addresses the neural correlates of stimuli that produce more complex patterns of pitch judgments, such as shifts in pitch and multiple pitches. Correlates of pitch shift and pitch ambiguity were investigated with the use of harmonic and inharmonic amplitude-modulated (AM) tones varying either in carrier frequency or modulation frequency. Pitches estimated from the pooled interval distributions showed shifts corresponding to "the first effect of pitch shift" (de Boer's rule) that is observed psychophysically. Pooled interval distributions in response to inharmonic stimulus segments showed multiple maxima corresponding to the multiple pitches heard by human listeners (pitch ambiguity). 3. AM and quasi-frequency-modulated tones with low carrier frequencies produce very similar patterns of pitch judgments, despite great differences in their phase spectra and waveform envelopes. Pitches estimated from pooled interval distributions were remarkably similar for the two kinds of stimuli, consistent with the psychophysically observed phase invariance of pitches produced by sets of low-frequency components. 4. Trains of clicks having uniform and alternating polarities were used to investigate the relation between pitches associated with periodicity and those associated with click rate. For unipolar click trains, where periodicity and rate coincide, physiologically estimated pitches closely follow the fundamental period. This corresponds to the pitch at the fundamental frequency (F0) that is heard. For alternating click trains, where rate and periodicity do not coincide, physiologically estimated pitches always closely followed the fundamental period. Although these pitch estimates corresponded to periodicity pitches that are heard for F0s > 150 Hz, they did not correspond to the rate pitches that are heard for F0s < 150 Hz. The predominant interval hypothesis thus failed to predict rate pitch. 5. When alternating-polarity click trains are high-pass filtered, rate pitches are strengthened and can also be heard at F0s > 150 Hz. Pitches for high-pass-filtered alternating click trains were estimated from pooled responses of fibers with characteristic frequencies (CFs) > 2 kHz. Roughly equal numbers of intervals at 1/rate and 1/F0 were found for all F0s studied, from 80 to 160 Hz, producing pitch estimates consistent with the rate pitches that are heard after high-pass filtering. The existence region for rate pitch also coincided with the presence of clear periodicities related to the click rate in pooled peristimulus time histograms. These periodicities were strongest for ensembles of fibers with CFs > 2 kHz, where there is widespread synchrony of discharges across many fibers. 6. The "dominance region for pitch" was studied with the use of two harmonic complexes consisting of harmonics 3-5 of one F0 and harmonics 6-12 of another fundamental 20% higher in frequency. When the complexes were presented individually, pitch estimates were always close to the fundamental of the complex. When the complexes were presented concurrently, pitch estimates always followed the fundamental of harmonics 3-5 for F0s of 150-480 Hz. For F0s of 125-150 Hz, pitch estimates followed one or the other fundamental, and for F0s < 125 Hz, pitch estimates followed the fundamental of harmonics 6-12. (ABSTRACT TRUNCATED)

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Response Adaptation of Medial Olivocochlear Neurons Is Minimal

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2381 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2381-2392 ◽

Cited By ~ 8

Author(s):

M. C. Brown

Keyword(s):

Firing Rate ◽

Auditory Nerve ◽

General Characteristic ◽

Nerve Fibers ◽

Short Term ◽

Percentage Decrease ◽

Short Term Adaptation ◽

Auditory Nerve Fibers ◽

Medial Olivocochlear

Response adaptation is a general characteristic of neurons. A number of studies have investigated the adaptation characteristics of auditory-nerve fibers, which send information to the brain about sound stimuli. However, there have been no previous adaptation studies of olivocochlear neurons, which provide efferent fibers to hair cells and auditory nerve dendrites in the auditory periphery. To study adaptation in efferent fibers, responses of single olivocochlear neurons were recorded to characteristic-frequency tones and noise, using anesthetized guinea pigs. To measure short-term adaptation, stimuli of 500 ms duration were presented, and the responses were displayed as peristimulus time histograms. These histograms showed regular peaks, indicating a “chopping” pattern of response. The rate during each chopping period as well as the general trend of the histogram could be well fit by an equation that expresses the firing rate as a sum of 1) a short-term adaptive rate that decays exponentially with time and 2) a constant steady-state rate. For the adaptation in medial olivocochlear (MOC) neurons, the average exponential time constant was 47 ms, which is roughly similar to that for short-term adaptation in auditory-nerve fibers. The amount of adaptation (expressed as a percentage decrease of onset firing rate), however, was substantially less in MOC neurons (average 31%) than in auditory-nerve fibers (average 63%). To test for adaptation over longer periods, we used noise and tones of 10 s duration. After the short-term adaptation, the responses of MOC neurons were almost completely sustained (average long-term adaptation 3%). However, in the same preparations, significant long-term adaptation was present in auditory-nerve fibers. These results indicate that the MOC response adaptation is minimal compared with that of auditory-nerve fibers. Such sustained responses may enable the MOC system to produce sustained effects in the periphery, supporting a role for this efferent system during ongoing stimuli of long duration.

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Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences

Journal of Neurophysiology ◽

10.1152/jn.1995.73.3.1043 ◽

1995 ◽

Vol 73 (3) ◽

pp. 1043-1062 ◽

Cited By ~ 183

Author(s):

P. X. Joris ◽

T. C. Yin

Keyword(s):

High Frequency ◽

Response Rate ◽

Discharge Rate ◽

Modulation Frequency ◽

Good Correspondence ◽

Afferent Pathways ◽

Lateral Superior Olive ◽

Interaural Time Differences ◽

Superior Olive ◽

Naturally Occurring

1. Interaural level differences (ILDs), created by the head and pinna, have long been known to be the dominant acoustic cue for azimuthal localization of high-frequency tones. However, psychophysical experiments have demonstrated that human subjects can also lateralize complex high-frequency sounds on the basis of interaural time differences (ITDs) of the signal envelope. The lateral superior olive (LSO) is one of two pairs of binaural nuclei where the primary extraction of binaural cues for sound source location occurs. "IE" cells in LSO are inhibited by stimuli to the contralateral and excited by stimuli to the ipsilateral ear, and their response rate is therefore dependent on ILD. Anatomic specializations in the afferent pathways to the LSO suggest that this circuit also has a function in the detection of timing cues. We hypothesized that, besides ILD sensitivity, the IE property also conveys a sensitivity to ITDs of amplitude-modulated (AM) tones and could provide the physiological substrate for the psychophysical effect mentioned above. 2. In extracellular recordings from binaural LSO cells in barbiturate-anesthetized cats, response rate was a periodic function of ITDs of AM stimuli, i.e., all cells displayed ITD sensitivity. Binaural responses were smaller than responses to stimulation of the ipsilateral ear alone and were minimal when the envelopes in both ears were in-phase or nearly so. There was good correspondence between responses to ITDs and to dynamic interaural phase differences (IPDs), created by a difference in the envelope frequency to the two ears. Qualitatively, the responses were consistent with the outcome of an IE operation on temporally structured inputs. 3. To compare the relative importance of ILD and ITD, responses to combinations of the two cues were obtained. Despite robust ITD sensitivity in all binaural LSO cells encountered, the changes in response rate that would occur in response to naturally occurring ITDs were small in comparison with the changes expected for naturally occurring ILDs. The main limitation on ITD sensitivity was a steep decline in average discharge rate as the modulation frequency exceeded several hundred Hertz. 4. ITD sensitivity was also present to broadband stimuli, again with minimal rates occurring near 0 ITD. The sensitivity depended in a predictable fashion on the passband of filtered noise and was absent to binaurally uncorrelated noise bands. In response to clicks, ILDs interacted with ITD in a complicated fashion involving amplitude and latency effects. 5. Three low-characteristic frequency (CF) LSO cells were encountered that were IE and showed ITD sensitivity to the fine structure of low-frequency stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

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Emergence of band-pass filtering through adaptive spiking in the owl's cochlear nucleus

Journal of Neurophysiology ◽

10.1152/jn.00132.2014 ◽

2014 ◽

Vol 112 (2) ◽

pp. 430-445 ◽

Cited By ~ 12

Author(s):

Bertrand Fontaine ◽

Katrina M. MacLeod ◽

Susan T. Lubejko ◽

Louisa J. Steinberg ◽

Christine Köppl ◽

...

Keyword(s):

Cochlear Nucleus ◽

Auditory Nerve ◽

Modulation Frequency ◽

Nerve Fibers ◽

Second Order ◽

Sound Recognition ◽

Fast Time ◽

Spike Threshold ◽

Auditory Nerve Fibers

In the visual, auditory, and electrosensory modalities, stimuli are defined by first- and second-order attributes. The fast time-pressure signal of a sound, a first-order attribute, is important, for instance, in sound localization and pitch perception, while its slow amplitude-modulated envelope, a second-order attribute, can be used for sound recognition. Ascending the auditory pathway from ear to midbrain, neurons increasingly show a preference for the envelope and are most sensitive to particular envelope modulation frequencies, a tuning considered important for encoding sound identity. The level at which this tuning property emerges along the pathway varies across species, and the mechanism of how this occurs is a matter of debate. In this paper, we target the transition between auditory nerve fibers and the cochlear nucleus angularis (NA). While the owl's auditory nerve fibers simultaneously encode the fast and slow attributes of a sound, one synapse further, NA neurons encode the envelope more efficiently than the auditory nerve. Using in vivo and in vitro electrophysiology and computational analysis, we show that a single-cell mechanism inducing spike threshold adaptation can explain the difference in neural filtering between the two areas. We show that spike threshold adaptation can explain the increased selectivity to modulation frequency, as input level increases in NA. These results demonstrate that a spike generation nonlinearity can modulate the tuning to second-order stimulus features, without invoking network or synaptic mechanisms.

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