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

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.

1985 ◽  
Vol 53 (1) ◽  
pp. 89-109 ◽  
Author(s):  
G. Harnischfeger ◽  
G. Neuweiler ◽  
P. Schlegel

Single-unit responses to tonal stimulation with interaural disparities were recorded in the nuclei of the superior olivary complex (SOC) and the central nucleus of the inferior colliculus (ICC) of the echolocating bat, Molossus ater. Seventy-six units were recorded from the ICC and 74 from the SOC; of the SOC units, 31 were histologically verified in the medial superior olive (MSO), 10 in the lateral superior olive (LSO), and 33 in unidentified areas of the SOC. Best frequencies (BFs) of the units ranged from 10.3 to 89.6 kHz, and Q10 dB values ranged from 2 to 70 dB. Most ICC neurons responded phasically to stimulus onset and were either inhibitory/excitatory [I/E; (53)] or excitatory/excitatory [E/E; (21)] units. In the MSO, 23 units responded tonically and 7 phasically on, 18 were E/E or E/OF (facilitatory for other input) units, and 11 were I/E neurons. All LSO neurons responded in a "chopper" fashion, and the binaural neurons were E/I units. In E/E units the excitatory response to binaural stimulation was frequently larger than the sum of the monaurally evoked responses. Many neurons with E/I or I/E inputs had very steep binaural impulse-count functions and were sensitive to small interaural intensity differences. Twenty-eight units (24%) responded with a change in firing rate of at least 20% to interaural time differences of +/- 500 microseconds. Within this sample, 11 units (8 from ICC, 2 from MSO, and 1 from SOC) were sensitive to interaural time differences of only +/- 50 microseconds. Of these 11 units, 10 were I/E units responding phasically only to stimulus onset and were also sensitive to intensity differences (delta I), being suppressed completely by the inhibitory input over a delta I range of 20 dB or less. Of 117 units tested in the ICC and SOC nuclei, 86 units (76%) were not sensitive to interaural time disparities within +/- 500 microseconds. Because the BFs of these units sensitive to interaural transient time differences (delta t) ranged between 18 and 90 kHz, responses were elicited by pure tones, and responses did not change periodically with the period equal to that of the stimulus frequency, we conclude that the neurons reacted to interaural differences of stimulus-onset time (transient time difference) but not to phase differences (ongoing time difference). Sensitivity to interaural time differences was also correlated with interaural intensity differences.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 69 (3) ◽  
pp. 842-859 ◽  
Author(s):  
E. Covey

1. Connectional evidence suggests that the dorsal nucleus of the lateral lemniscus (DNLL) and the paralemniscal zone (PL) function as centers for binaural analysis interposed between the superior olivary complex and the midbrain. In addition, the DNLL is known to be a major source of inhibitory input to the midbrain. The aim of this study was to characterize the response properties of neurons in DNLL and PL of the echolocating bat Eptesicus fuscus, a species that utilizes high-frequency hearing and that might be expected to have a large proportion of neurons responsive to interaural differences in sound level. 2. Auditory stimuli were presented monaurally or binaurally to awake animals, and responses of single units were recorded extra-cellularly with the use of glass micropipettes. 3. Below the ventrolateral border of the inferior colliculus is a region that contains large gamma-aminobutyric acid-positive neurons. On the basis of its immunohistochemical reactivity, this entire region could be considered as DNLL. However, within the area, there was an uneven distribution of binaural responses. Caudally, binaural neurons made up 84% (41/49) of those tested, but rostrally only 29% (6/21). For this reason the rostral area is considered as a separate functional subdivision and referred to as the dorsal paralemniscal zone (DPL). PL is located ventral to DPL and medial to the intermediate and ventral nuclei of the lateral lemniscus; in PL 88% (14/16) of neurons were binaural. 4. Most neurons responded only to a contralateral stimulus when sounds were presented monaurally. Out of 49 neurons in DNLL, 42 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 6 responded to sound at either ear. In the DPL, all of the 21 neurons tested responded to a contralateral sound and none to an ipsilateral sound. Out of 16 neurons in the PL, 11 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 4 responded to sound at either ear. 5. When sounds were presented at both ears simultaneously, several different patterns of binaural interaction occurred. The most common pattern was suppression of the response to sound at one ear by sound at the other ear. In DNLL, 57% (28/49) of neurons showed this type of binaural interaction. Another 10% (5/49) showed facilitation at some interaural level differences and suppression at others, and another 10% (5/49) showed facilitation at some interaural level differences but no suppression.(ABSTRACT TRUNCATED AT 400 WORDS)


Author(s):  
Felix Felmy

Parallel processing streams guide ascending auditory information through the processing hierarchy of the auditory brainstem. Many of these processing streams converge in the lateral lemnisucus, the fiber bundle that connects the cochlear nuclei and superior olivary complex with the inferior colliculus. The neuronal populations within the lateral lemniscus can be segregated according to their gross structure-function relationships into three distinct nuclei. These nuclei are termed ventral, intermedial, and dorsal nucleus, according to their position within the lemniscal fiber bundle. The complexity of their input pattern increases in an ascending fashion. The three nuclei employ different neurotransmitters and exhibit distinct synaptic and biophysical features. Yet they all share a large heterogeneity. Functionally, the ventral nucleus of the lateral lemniscus has been hypothesized to reduce spectral splatter by generating a rapid, temporally precise feedforward onset inhibition in the inferior colliculus. In the intermedial nucleus of the lateral lemniscus a cross-frequency integration has been observed. The hallmark of the dorsal nucleus of the lateral lemniscus is the generation of a long-lasting inhibition in its contralateral counterpart and the inferior colliculus. This inhibition is proposed to generate a suppression of sound sources during reverberations and could act as a temporal filter capable of removing spurious interaural time differences. While great advances have been made in understanding the role that these nuclei play in auditory processing, the functional diversity of the individual neuronal responsiveness within each nucleus remains largely unsolved.


2021 ◽  
Vol 15 ◽  
Author(s):  
Sharonda Harris ◽  
Renee Afram ◽  
Takashi Shimano ◽  
Bozena Fyk-Kolodziej ◽  
Paul D. Walker ◽  
...  

Dopamine (DA) modulates the activity of nuclei within the ascending and descending auditory pathway. Previous studies have identified neurons and fibers in the inferior colliculus (IC) which are positively labeled for tyrosine hydroxylase (TH), a key enzyme in the synthesis of dopamine. However, the origins of the tyrosine hydroxylase positive projections to the inferior colliculus have not been fully explored. The lateral lemniscus (LL) provides a robust inhibitory projection to the inferior colliculus and plays a role in the temporal processing of sound. In the present study, immunoreactivity for tyrosine hydroxylase was examined in animals with and without 6-hydroxydopamine (6-OHDA) lesions. Lesioning, with 6-OHDA placed in the inferior colliculus, led to a significant reduction in tyrosine hydroxylase immuno-positive labeling in the lateral lemniscus and inferior colliculus. Immunolabeling for dopamine beta-hydroxylase (DBH) and phenylethanolamine N-methyltransferase (PNMT), enzymes responsible for the synthesis of norepinephrine (NE) and epinephrine (E), respectively, were evaluated. Very little immunoreactivity for DBH and no immunoreactivity for PNMT was found within the cell bodies of the dorsal, intermediate, or ventral nucleus of the lateral lemniscus. The results indicate that catecholaminergic neurons of the lateral lemniscus are likely dopaminergic and not noradrenergic or adrenergic. Next, high-pressure liquid chromatography (HPLC) analysis was used to confirm that dopamine is present in the inferior colliculus and nuclei that send projections to the inferior colliculus, including the cochlear nucleus (CN), superior olivary complex (SOC), lateral lemniscus, and auditory cortex (AC). Finally, fluorogold, a retrograde tracer, was injected into the inferior colliculus of adult rats. Each subdivision of the lateral lemniscus contained fluorogold within the somata, with the dorsal nucleus of the lateral lemniscus showing the most robust projections to the inferior colliculus. Fluorogold-tyrosine hydroxylase colocalization within the lateral lemniscus was assessed. The dorsal and intermediate nuclei neurons exhibiting similar degrees of colocalization, while neurons of the ventral nucleus had significantly fewer colocalized fluorogold-tyrosine hydroxylase labeled neurons. These results suggest that several auditory nuclei that project to the inferior colliculus contain dopamine, dopaminergic neurons in the lateral lemniscus project to the inferior colliculus and that dopaminergic neurotransmission is poised to play a pivotal role in the function of the inferior colliculus.


1989 ◽  
Vol 61 (2) ◽  
pp. 257-268 ◽  
Author(s):  
R. Batra ◽  
S. Kuwada ◽  
T. R. Stanford

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)


2007 ◽  
Vol 98 (5) ◽  
pp. 2705-2715 ◽  
Author(s):  
Ida Siveke ◽  
Christian Leibold ◽  
Benedikt Grothe

We are regularly exposed to several concurrent sounds, producing a mixture of binaural cues. The neuronal mechanisms underlying the localization of concurrent sounds are not well understood. The major binaural cues for localizing low-frequency sounds in the horizontal plane are interaural time differences (ITDs). Auditory brain stem neurons encode ITDs by firing maximally in response to “favorable” ITDs and weakly or not at all in response to “unfavorable” ITDs. We recorded from ITD-sensitive neurons in the dorsal nucleus of the lateral lemniscus (DNLL) while presenting pure tones at different ITDs embedded in noise. We found that increasing levels of concurrent white noise suppressed the maximal response rate to tones with favorable ITDs and slightly enhanced the response rate to tones with unfavorable ITDs. Nevertheless, most of the neurons maintained ITD sensitivity to tones even for noise intensities equal to that of the tone. Using concurrent noise with a spectral composition in which the neuron's excitatory frequencies are omitted reduced the maximal response similar to that obtained with concurrent white noise. This finding indicates that the decrease of the maximal rate is mediated by suppressive cross-frequency interactions, which we also observed during monaural stimulation with additional white noise. In contrast, the enhancement of the firing rate to tones at unfavorable ITD might be due to early binaural interactions (e.g., at the level of the superior olive). A simple simulation corroborates this interpretation. Taken together, these findings suggest that the spectral composition of a concurrent sound strongly influences the spatial processing of ITD-sensitive DNLL neurons.


1997 ◽  
Vol 77 (1) ◽  
pp. 324-340 ◽  
Author(s):  
Lichuan Yang ◽  
George D. Pollak

Yang, Lichuan and George D. Pollak. Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J. Neurophysiol. 77: 324–340, 1997. We studied the phase-locking of 89 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat to sinusoidally amplitude modulated (SAM) signals and the influence that GABAergic inhibition had on their response properties. Response properties were determined with tone bursts at each neuron's best frequency and then with a series of SAM signals that had modulation frequencies ranging from 50–100 to 800 Hz in 100-Hz steps. DNLL neurons were divided into two principal types: sustained neurons (55%), which responded throughout the duration of the tone burst, and onset neurons (45%), which responded only at the beginning of the tone burst. Sustained and onset neurons responded differently to SAM signals. Sustained neurons responded with phase-locked discharges to modulation frequencies ≤400–800 Hz. In contrast, 70% of the onset neurons phase-locked only to low modulation frequencies of 100–300 Hz, whereas 30% of the onset neurons did not phase-lock to any modulation frequency. Signal intensity differentially affected the phase-locking of sustained and onset neurons. Sustained neurons exhibited tight phase-locking only at low intensities, 10–30 dB above threshold. Onset neurons, in contrast, maintained strong phase-locking even at relatively high intensities. Blocking GABAergic inhibition with bicuculline had different effects on the phase-locking of sustained and onset neurons. In sustained neurons, there was an overall decline in phase-locking at all modulation frequencies. In contrast, 70% of the onset neurons phase-locked to much higher modulation frequencies than they did when inhibition was intact. The other 30% of onset neurons phase-locked to SAM signals, although they fired only with an onset response to the same signals before inhibition was blocked. In both cases, blocking GABAergic inhibition transformed their responses to SAM signals into patterns that were more like those of sustained neurons. We also propose mechanisms that could explain the differential effects of GABAergic inhibition on onset neurons that locked to low modulation frequencies and on onset neurons that did not lock to any SAM signals before inhibition was blocked. The key features of the proposed mechanisms are the absolute latencies and temporal synchrony of the excitatory and inhibitory inputs.


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