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

1995 ◽  
Vol 73 (3) ◽  
pp. 1043-1062 ◽  
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)

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

1998 ◽  
Vol 79 (1) ◽  
pp. 253-269 ◽  
Author(s):  
Philip X. Joris ◽  
Tom C. T. Yin
Keyword(s):  
Firing Rate ◽  
Auditory Nerve ◽  
Modulation Frequency ◽  
Nerve Fibers ◽  
Cell Populations ◽  
Average Firing Rate ◽  
Afferent Pathways ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Auditory Nerve Fibers

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.

Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive

1996 ◽  
Vol 76 (4) ◽  
pp. 2137-2156 ◽  
Author(s):  
P. X. Joris
Keyword(s):  
Modulation Frequency ◽  
Small Sample ◽  
Spike Rate ◽  
Common Mechanism ◽  
Half Cycle ◽  
Medial Superior Olive ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Binaural Interaction ◽  
Interaural Phase

1. Spike rates of cells in the cat's lateral superior olive (LSO) depend on interaural level differences (ILDs) and envelope interaural time differences (ITDs) of amplitude-modulated tones presented to both ears. We previously proposed that these sensitivities arise from a common mechanism, which is the IE binaural interaction (Inhibited by the contralateral and Excited by the ipsilateral ear). As a further test of that proposal and to gain a better understanding of the importance of this ITD-sensitivity, responses to monaural and binaural modulation are compared here over a range of modulation frequencies. 2. At low modulation frequencies, LSO-IE cells respond maximally when the envelopes of the amplitude-modulated stimuli at the two ears are out-of-phase by a half-cycle. This phase difference changes in a systematic way, which varies from cell to cell, when modulation frequency is increased. Mean interaural phase, measured over a range of modulation frequencies, was subjected to a characteristic delay analysis. Two measures were extracted: characteristic delay, which reflects differences in conduction delay between ipsi- and contralateral pathways, and characteristic phase, which reflects their sign of interaction. Most characteristic delays were within the physiological range of ITDs. There was a small bias toward positive delays, indicating a longer conduction time for the contralateral pathway. Characteristic phases were tightly distributed approximately 0.5 cycles, consistent with the proposed IE mechanism for ITD-sensitivity. 3. Increases in the modulation frequency of binaural stimuli beyond approximately 300 Hz consistently caused a profound decrease in average spike rate, as well as a decrease in the modulation of spike rate by ITD. The upper limit of ITD-sensitivity was 800 Hz. Sensitivity to envelope ITDs therefore is limited to a much lower range of frequencies than sensitivity to ITDs in fine-structure, e.g., as found in the medial superior olive (MSO), which operates up to several kilo Hertz. 4. A small sample of high-frequency EE cells (excited by both ears) in MSO also was tested with binaural amplitude-modulated stimuli. MSO-EE cells showed weak envelope ITD-sensitivity over a limited range of modulation frequencies. Consistent with the EE interaction, characteristic phases clustered approximately 0 cycles. 5. Mean interaural phase was compared with the phase of responses to monaural modulation. The difference between the ipsilateral and contralateral phases correlated well with the phase measured binaurally, both for LSO and MSO cells. 6. Many features of LSO-IE responses were mimicked by the simplest possible computer model, consisting of subtraction and rectification of low-pass filtered envelope waveforms. Differences between model and physiological results are suggestive of a temporal limitation in the binaural interaction that creates the ITD-sensitivity. 7. These results provide additional evidence for LSO ITD-sensitivity paralleling human psychophysical results. The stimulus boundaries within which ITD-sensitivity occurs suggest that it has a limited role in free-field conditions. It is traditionally thought that, to contribute to the perceived change in spatial location of a sound source, the LSO needs to show a change in overall firing rate summed across cells. This is achieved with small ILDs, but requires large ITDs, because the latter cue is less potent in single cells and has varied effects across cells by virtue of differences in characteristic delay.

Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition

1991 ◽  
Vol 65 (3) ◽  
pp. 598-605 ◽  
Author(s):  
P. G. Finlayson ◽  
D. M. Caspary
Keyword(s):  
Discharge Rate ◽  
Low Frequency ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Total Inhibition ◽  
Interaural Phase ◽  
Phase Sensitive ◽  
Evoked Activity ◽  
Discharge Patterns ◽  
Contralateral Stimulus

1. Responses of low characteristic frequency (CF) neurons in the lateral limb of the lateral superior olive (LSO) of chinchilla and rat to binaural stimuli at various interaural phase and intensity differences were examined and compared to responses from previous studies of high CF neurons. 2. Ninety-six LSO neurons from chinchillas and 10 LSO neurons from rats with CFs less than 1,200 Hz were characterized. The majority of these neurons displayed phase-locked tone-evoked temporal discharge patterns to ipsilateral CF stimuli. 3. Similar to high-CF LSO neurons, low-CF LSO neurons were excited by ipsilateral stimuli and inhibited by contralateral stimuli, with discharge rate sensitive to interaural intensity differences (IID). Discharge rate increased as ipsilateral intensity was increased and decreased as contralateral stimulus intensity was increased. 4. Binaural inhibition, inhibition of ipsilaterally evoked activity by contralateral stimuli, was dependent on interaural phase differences (IPD) in the majority of low-CF LSO neurons. Responses of phase-sensitive neurons to binaural stimuli often varied with 90 or 180 degrees changes in IPD from total inhibition to a facilitated response when compared to responses to control ipsilateral stimuli alone. 5. In summary, like high-CF LSO neurons, LSO neurons with low CFs (less than 1,200 Hz) were ipsilaterally excited and contralaterally inhibited (EI) and were sensitive to IID. Unlike most high-CF EI LSO neurons, which are not responsive when the azimuth of the stimulus is directly in front of or directly behind the animal, many low-CF LSO neurons are responsive to these stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Dual sensitivity of inferior colliculus neurons to ITD in the envelopes of high-frequency sounds: experimental and modeling study

2014 ◽  
Vol 111 (1) ◽  
pp. 164-181 ◽  
Author(s):  
Le Wang ◽  
Sasha Devore ◽  
Bertrand Delgutte ◽  
H. Steven Colburn
Keyword(s):  
Simple Model ◽  
Computational Model ◽  
Inferior Colliculus ◽  
Sound Localization ◽  
High Frequency ◽  
Modulation Frequency ◽  
Primary Site ◽  
Interaural Time Differences ◽  
Binaural Interaction ◽  
Unanesthetized Rabbit

Human listeners are sensitive to interaural time differences (ITDs) in the envelopes of sounds, which can serve as a cue for sound localization. Many high-frequency neurons in the mammalian inferior colliculus (IC) are sensitive to envelope-ITDs of sinusoidally amplitude-modulated (SAM) sounds. Typically, envelope-ITD-sensitive IC neurons exhibit either peak-type sensitivity, discharging maximally at the same delay across frequencies, or trough-type sensitivity, discharging minimally at the same delay across frequencies, consistent with responses observed at the primary site of binaural interaction in the medial and lateral superior olives (MSO and LSO), respectively. However, some high-frequency IC neurons exhibit dual types of envelope-ITD sensitivity in their responses to SAM tones, that is, they exhibit peak-type sensitivity at some modulation frequencies and trough-type sensitivity at other frequencies. Here we show that high-frequency IC neurons in the unanesthetized rabbit can also exhibit dual types of envelope-ITD sensitivity in their responses to SAM noise. Such complex responses to SAM stimuli could be achieved by convergent inputs from MSO and LSO onto single IC neurons. We test this hypothesis by implementing a physiologically explicit, computational model of the binaural pathway. Specifically, we examined envelope-ITD sensitivity of a simple model IC neuron that receives convergent inputs from MSO and LSO model neurons. We show that dual envelope-ITD sensitivity emerges in the IC when convergent MSO and LSO inputs are differentially tuned for modulation frequency.

scholarly journals Discharge patterns in the lateral superior olive of decerebrate cats

2012 ◽  
Vol 108 (7) ◽  
pp. 1942-1953 ◽  
Author(s):  
Nathaniel T. Greene ◽  
Kevin A. Davis
Keyword(s):  
Discharge Rate ◽  
Full Range ◽  
Stimulus Onset ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Shape Adaptation ◽  
Discharge Patterns ◽  
Decerebrate Cats ◽  
Sustained Discharge ◽  
Initial Peak

Anatomical and pharmacological studies have shown that the lateral superior olive (LSO) receives inputs from a number of sources and that LSO cells can alter the balance of their own excitatory and inhibitory drive. It is thus likely that the ongoing sound-evoked responses of LSO cells reflect a complex interplay of excitatory and inhibitory events, which may be affected by anesthesia. The goal of this study was to characterize the temporal discharge patterns of single units in the LSO of unanesthetized, decerebrate cats in response to long-duration ipsilateral best-frequency tone bursts. A decision tree is presented to partition LSO units on the basis of poststimulus time histogram shape, adaptation of instantaneous firing rate as a function of time, and sustained discharge rate. The results suggest that LSO discharge patterns form a continuum with four archetypes: sustained choppers that show two or more peaks of activity at stimulus onset and little adaptation of rate throughout the response, transient choppers that undergo a decrease in rate that eventually stabilizes with time, primary-like units that display an initial peak of activity followed by a monotonic decline in rate to a steady-state value, and onset-sustained units that exhibit an initial peak of activity at stimulus onset followed by a low sustained activity. Compared with the chopper units, the nonchopper units tend to show longer first-spike latencies, lower peak firing rates, and more irregular sustained discharge patterns. Modeling studies show that the full range of LSO response types can be obtained from an underlying sustained chopper by varying the strength and latency of a sound-driven ipsilateral inhibition relative to that of excitation. Together, these results suggest that inhibition plays a major role in shaping the temporal discharge patterns of units in unanesthetized preparations.

Effects of Amplitude Modulation on the Coding of Interaural Time Differences of Low-Frequency Sounds in the Inferior Colliculus. I. Response Properties

2003 ◽  
Vol 90 (5) ◽  
pp. 2818-2826 ◽  
Author(s):  
S. J. Sterbing ◽  
W. R. D'Angelo ◽  
E.-M. Ostapoff ◽  
S. Kuwada
Keyword(s):  
Inferior Colliculus ◽  
Amplitude Modulation ◽  
Discharge Rate ◽  
Modulation Frequency ◽  
Low Frequency ◽  
The Other ◽  
Neuronal Responses ◽  
Frequency Range ◽  
Interaural Time Differences ◽  
Tuning Width

Most sounds in the natural environment are amplitude-modulated (AM). To determine if AM alters the neuronal sensitivity to interaural time differences (ITDs) in low-frequency sounds, we tested neuronal responses to a binaural beat stimulus with and without modulation. We recorded from single units in the inferior colliculus of the unanesthetized rabbit. We primarily used low frequency (∼25 Hz) modulation that was identical at both ears. We found that modulation could enhance, suppress, or not affect the discharge rate. In extreme cases, a neuron that showed no response to the unmodulated binaural beat did so when modulation was added to both ears. At the other extreme, a neuron that showed sensitivity to the unmodulated binaural beat ceased firing with modulation. Modulation could also affect the frequency range of ITD sensitivity, best ITD, and ITD tuning width. Despite these changes in individual neurons, averaging across all neurons, the peak and width of the population ITD function remained unchanged. Because ITD-sensitive neurons also time-locked to the modulation frequency, the location and sound attributes are processed simultaneously by these neurons.

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