A comparison of the interaural time sensitivity of neurons in the inferior colliculus and thalamus of the unanesthetized rabbit

1. The difference in the time of arrival of a sound at the two ears can be used to locate its source along the azimuth. Traditionally, it has been thought that only the on-going interaural temporal disparities (ITDs) produced by sounds of lower frequency (approximately less than 2 kHz) could be used for this purpose. However, ongoing ITDs of low frequency are also produced by envelopes of amplitude-modulated (AM) tones. These ITDs can be detected and used to lateralize complex high-frequency sounds (1, 8, 12, 15, 22, 24, 26). Auditory neurons synchronize to the modulation envelope, but do so at progressively lower modulation frequencies at higher levels of the auditory pathway. Some neurons of the cochlear nucleus synchronize best to frequencies as high as 700 Hz, but those of the inferior colliculus (IC) exhibit their best synchrony below 200 Hz. Even though synchrony to higher modulation frequencies is reduced at higher levels of the auditory pathway, is information about ITDs retained? 2. We answered this question by extracellularly recording the responses of neurons in the IC of the unanesthetized rabbit. We used an unanesthetized preparation because anesthesia alters the responses of neurons in the IC to both monaurally presented tones and ITDs. The unanesthetized rabbit is ideal for auditory research. Recordings can be maintained for long periods, and the acoustic stimulus to each ear can be independently controlled. 3. We studied the responses of 89 units to sinusoidally AM tones presented to the contralateral ear. For each unit, we recorded the response at several modulation frequencies. The degree of phase locking to the envelope at each frequency was measured using the synchronization coefficient. Two measures were used to assess the range of modulation frequencies over which phase locking occurred. The "best AM frequency" was the frequency at which we observed the greatest phase locking. The "highest AM frequency" was the highest frequency at which significant phase locking (0.001 level) was observed. We could not assess synchrony to ipsilateral AM tones directly, because most units did not respond to ipsilateral stimulation. 4. We studied the sensitivity of 63 units to ITDs produced by the envelopes of AM tones. Sensitivity to ITDs was tested by presenting AM tones to the two ears that had the same carrier frequency, but modulation frequencies that differed by 1 Hz. Units that were sensitive to ITDs responded to this stimulus by varying their response rate cyclically at the difference frequency, i.e., 1 Hz.(ABSTRACT TRUNCATED AT 400 WORDS)

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Azimuth and envelope coding in the inferior colliculus of the unanesthetized rabbit: effect of reverberation and distance

Journal of Neurophysiology ◽

10.1152/jn.00826.2013 ◽

2014 ◽

Vol 112 (6) ◽

pp. 1340-1355 ◽

Cited By ~ 10

Author(s):

Shigeyuki Kuwada ◽

Brian Bishop ◽

Duck O. Kim

Keyword(s):

Inferior Colliculus ◽

Auditory System ◽

Neural Coding ◽

Neural Responses ◽

Auditory Space ◽

Unanesthetized Rabbit ◽

Reverberant Environments ◽

Monaural Stimulation ◽

Neural Gain

Recognition and localization of a sound are the major functions of the auditory system. In real situations, the listener and different degrees of reverberation transform the signal between the source and the ears. The present study was designed to provide these transformations and examine their influence on neural responses. Using the virtual auditory space (VAS) method to create anechoic and moderately and highly reverberant environments, we found the following: 1) In reverberation, azimuth tuning was somewhat degraded with distance whereas the direction of azimuth tuning remained unchanged. These features remained unchanged in the anechoic condition. 2) In reverberation, azimuth tuning and envelope synchrony were degraded most for neurons with low best frequencies and least for neurons with high best frequencies. 3) More neurons showed envelope synchrony to binaural than to monaural stimulation in both anechoic and reverberant environments. 4) The percentage of envelope-coding neurons and their synchrony decreased in reverberation with distance, whereas it remained constant in the anechoic condition. 5) At far distances, for both binaural and monaural stimulation, the neural gain in reverberation could be as high as 30 dB and as much as 10 dB higher than those in the anechoic condition. 6) The majority of neurons were able to code both envelope and azimuth in all of the environments. This study provides a foundation for understanding the neural coding of azimuth and envelope synchrony at different distances in reverberant and anechoic environments. This is necessary to understand how the auditory system processes “where” and “what” information in real environments.

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Detection of interaural correlation by neurons in the superior olivary complex, inferior colliculus and auditory cortex of the unanesthetized rabbit

Hearing Research ◽

10.1016/j.heares.2006.06.005 ◽

2006 ◽

Vol 221 (1-2) ◽

pp. 1-16 ◽

Cited By ~ 30

Author(s):

Charles S. Coffey ◽

Charles S. Ebert ◽

Allen F. Marshall ◽

John D. Skaggs ◽

Stephanie E. Falk ◽

...

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Superior Olivary Complex ◽

Unanesthetized Rabbit ◽

Interaural Correlation

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Changes in interaural time sensitivity with interaural level differences in the inferior colliculus

Hearing Research ◽

10.1016/j.heares.2006.10.005 ◽

2007 ◽

Vol 223 (1-2) ◽

pp. 105-113 ◽

Cited By ~ 10

Author(s):

Alan R. Palmer ◽

Liang-fa Liu ◽

Trevor M. Shackleton

Keyword(s):

Inferior Colliculus ◽

Time Sensitivity ◽

Interaural Level Differences

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

The Journal of the Acoustical Society of America ◽

10.1121/1.391457 ◽

1984 ◽

Vol 76 (5) ◽

pp. 1401-1410 ◽

Cited By ~ 56

Author(s):

Tom C. T. Yin ◽

Shigeyuki Kuwada ◽

Yasumasa Sujaku

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Time Sensitivity

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

Journal of Neurophysiology ◽

10.1152/jn.00450.2013 ◽

2014 ◽

Vol 111 (1) ◽

pp. 164-181 ◽

Cited By ~ 14

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.

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Sensitivity to Interaural Time Differences in the Dorsal Nucleus of the Lateral Lemniscus of the Unanesthetized Rabbit: Comparison With Other Structures

Journal of Neurophysiology ◽

10.1152/jn.00901.2005 ◽

2006 ◽

Vol 95 (3) ◽

pp. 1309-1322 ◽

Cited By ~ 25

Author(s):

Shigeyuki Kuwada ◽

Douglas C. Fitzpatrick ◽

Ranjan Batra ◽

Ernst-Michael Ostapoff

Keyword(s):

Inferior Colliculus ◽

Phase Locking ◽

Large Majority ◽

Superior Olivary Complex ◽

Inhibitory Input ◽

Lateral Lemniscus ◽

Interaural Time Differences ◽

Auditory Thalamus ◽

Dorsal Nucleus ◽

Unanesthetized Rabbit

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.

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Spatial tuning to sound-source azimuth in the inferior colliculus of unanesthetized rabbit

Journal of Neurophysiology ◽

10.1152/jn.00532.2011 ◽

2011 ◽

Vol 106 (5) ◽

pp. 2698-2708 ◽

Cited By ~ 9

Author(s):

Shigeyuki Kuwada ◽

Brian Bishop ◽

Caitlin Alex ◽

Daniel W. Condit ◽

Duck O. Kim

Keyword(s):

Inferior Colliculus ◽

Sound Source ◽

Neural Coding ◽

Full Range ◽

Sound Field ◽

Stimulus Level ◽

Unanesthetized Rabbit ◽

Binaural Stimulation ◽

Wide Range ◽

Contralateral Ear

Despite decades of research devoted to the study of inferior colliculus (IC) neurons' tuning to sound-source azimuth, there remain many unanswered questions because no previous study has examined azimuth tuning over a full range of 360° azimuths at a wide range of stimulus levels in an unanesthetized preparation. Furthermore, a comparison of azimuth tuning to binaural and contralateral ear stimulation over ranges of full azimuths and widely varying stimulus levels has not previously been reported. To fill this void, we have conducted a study of azimuth tuning in the IC of the unanesthetized rabbit over a 300° range of azimuths at stimulus levels of 10–50 dB above neural threshold to both binaural and contralateral ear stimulation using virtual auditory space stimuli. This study provides systematic evidence for neural coding of azimuth. We found the following: 1) level-tolerant azimuth tuning was observed in the top 35% regarding vector strength and in the top 15% regarding vector angle of IC neurons; 2) preserved azimuth tuning to binaural stimulation at high stimulus levels was created as a consequence of binaural facilitation in the contralateral sound field and binaural suppression in the ipsilateral sound field; 3) the direction of azimuth tuning to binaural stimulation was primarily in the contralateral sound field, and its center shifted laterally toward −90° with increasing stimulus level; 4) at 10 dB, azimuth tuning to binaural and contralateral stimulation was similar, indicating that it was mediated by monaural mechanisms; and 5) at higher stimulus levels, azimuth tuning to contralateral ear stimulation was severely degraded. These findings form a foundation for understanding neural mechanisms of localizing sound-source azimuth.

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