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

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.

2011 ◽  
Vol 106 (2) ◽  
pp. 974-985 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young

Previous studies have demonstrated that single neurons in the central nucleus of the inferior colliculus (ICC) are sensitive to multiple sound localization cues. We investigated the hypothesis that ICC neurons are specialized to encode multiple sound localization cues that are aligned in space (as would naturally occur from a single broadband sound source). Sound localization cues including interaural time differences (ITDs), interaural level differences (ILDs), and spectral shapes (SSs) were measured in a marmoset monkey. Virtual space methods were used to generate stimuli with aligned and misaligned combinations of cues while recording in the ICC of the same monkey. Mutual information (MI) between spike rates and stimuli for aligned versus misaligned cues were compared. Neurons with best frequencies (BFs) less than ∼11 kHz mostly encoded information about a single sound localization cue, ITD or ILD depending on frequency, consistent with the dominance of ear acoustics by either ITD or ILD at those frequencies. Most neurons with BFs >11 kHz encoded information about multiple sound localization cues, usually ILD and SS, and were sensitive to their alignment. In some neurons MI between stimuli and spike responses was greater for aligned cues, while in others it was greater for misaligned cues. If SS cues were shifted to lower frequencies in the virtual space stimuli, a similar result was found for neurons with BFs <11 kHz, showing that the cue interaction reflects the spectra of the stimuli and not a specialization for representing SS cues. In general the results show that ICC neurons are sensitive to multiple localization cues if they are simultaneously present in the frequency response area of the neuron. However, the representation is diffuse in that there is not a specialization in the ICC for encoding aligned sound localization cues.


2020 ◽  
Vol 123 (5) ◽  
pp. 1791-1807 ◽  
Author(s):  
Ryan Dorkoski ◽  
Kenneth E. Hancock ◽  
Gareth A. Whaley ◽  
Timothy R. Wohl ◽  
Noelle C. Stroud ◽  
...  

A “division of labor” has previously been assumed in which the directions of low- and high-frequency sound sources are thought to be encoded by neurons preferentially sensitive to low and high frequencies, respectively. Contrary to this, we found that auditory midbrain neurons encode the directions of both low- and high-frequency sounds regardless of their preferred frequencies. Neural responses were shaped by different sound localization cues depending on the stimulus spectrum—even within the same neuron.


2008 ◽  
Vol 99 (5) ◽  
pp. 2390-2407 ◽  
Author(s):  
Zachary M. Smith ◽  
Bertrand Delgutte

Bilateral cochlear implantation seeks to improve hearing by taking advantage of the binaural processing of the central auditory system. Cochlear implants typically encode sound in each spectral channel by amplitude modulating (AM) a fixed-rate pulse train, thus interaural time differences (ITD) are only delivered in the envelope. We investigated the ITD sensitivity of inferior colliculus (IC) neurons with sinusoidally AM pulse trains. ITD was introduced independently to the AM and/or carrier pulses to measure the relative efficacy of envelope and fine structure for delivering ITD information. We found that many IC cells are sensitive to ITD in both the envelope (ITDenv) and fine structure (ITDfs) for appropriate modulation frequencies and carrier rates. ITDenv sensitivity was generally similar to that seen in normal-hearing animals with AM tones. ITDenv tuning generally improved with increasing modulation frequency up to the maximum modulation frequency that elicited a sustained response in a neuron (tested ≤160 Hz). ITDfs sensitivity was present in about half the neurons for 1,000 pulse/s (pps) carriers and was nonexistent at 5,000 pps. The neurons that were sensitive to ITDfs at 1,000 pps were those that showed the best ITD sensitivity to low-rate pulse trains. Overall, the best ITD sensitivity was found for ITD contained in the fine structure of a moderate rate AM pulse train (1,000 pps). These results suggest that the interaural timing of current pulses should be accurately controlled in a bilateral cochlear implant processing strategy that provides salient ITD cues.


2006 ◽  
Vol 95 (3) ◽  
pp. 1309-1322 ◽  
Author(s):  
Shigeyuki Kuwada ◽  
Douglas C. Fitzpatrick ◽  
Ranjan Batra ◽  
Ernst-Michael Ostapoff

Interaural time differences, a cue for azimuthal sound location, are first encoded in the superior olivary complex (SOC), and this information is then conveyed to the dorsal nucleus of the lateral lemniscus (DNLL) and inferior colliculus (IC). The DNLL provides a strong inhibitory input to the IC and may serve to transform the coding of interaural time differences (ITDs) in the IC. Consistent with the projections from the SOC, the DNLL and IC had similar distributions of peak- and trough-type neurons, characteristic delays, and best ITDs. The ITD tuning widths of DNLL neurons were intermediate between those of the SOC and IC. Further sharpening is seen in the auditory thalamus, indicating that sharpening mechanisms are not restricted to the midbrain. The proportion of neurons that phase-locked to the tones delivered to each ear progressively decreased from the SOC to the auditory thalamus. The degree of phase-locking for a large majority of DNLL neurons was too weak to support their involvement in processing monaural inputs to generate a sensitivity to ITDs. The response rates of DNLL neurons were on average ∼60% greater than in the IC or SOC, indicating that the inhibitory input provided to the IC by the DNLL is robust.


1995 ◽  
Vol 73 (3) ◽  
pp. 1043-1062 ◽  
Author(s):  
P. X. Joris ◽  
T. C. Yin

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)


2003 ◽  
Vol 90 (5) ◽  
pp. 2818-2826 ◽  
Author(s):  
S. J. Sterbing ◽  
W. R. D'Angelo ◽  
E.-M. Ostapoff ◽  
S. Kuwada

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.


2005 ◽  
Vol 93 (6) ◽  
pp. 3463-3478 ◽  
Author(s):  
Sarah J. Griffin ◽  
Leslie R. Bernstein ◽  
Neil J. Ingham ◽  
David McAlpine

Interaural time differences (ITDs) are important cues for mammalian sound localization. At high frequencies, sensitivity to ITDs, which are conveyed only by the envelope of the waveforms, has been shown to be poorer than sensitivity to ITDs at low frequencies, which are conveyed primarily by the fine structure of the waveforms. Recently, human psychophysical experiments have demonstrated that sensitivity to envelope-based ITDs in high-frequency transposed tones can be equivalent to low-frequency fine-structure–based ITD sensitivity. Transposed tones are designed to provide high-frequency auditory nerve fibers (ANFs) with similar temporal information to that provided by low-frequency tones. We investigated neural sensitivity to ITDs in high-frequency transposed and sinusoidally amplitude modulated (SAM) tones, in the inferior colliculus of the guinea pig. Neural sensitivity to ITDs in transposed tones was found to be greater than that to ITDs in SAM tones; in response to transposed tones, neural firing rates were more modulated as a function of ITD and discrimination thresholds were found to be lower than those in response to SAM tones. Similar to psychophysical findings, ITD discrimination of single neurons in response to transposed tones for rates of modulation <250 Hz was comparable to neural discrimination of ITDs in low-frequency tones. This suggests that the neural mechanisms that mediate sensitivity to ITDs at high and low frequencies are functionally equivalent, provided that the stimuli result in appropriate temporal patterns of action potentials in ANFs.


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