Two sources of inhibition affecting binaural evoked responses in the rat's inferior colliculus : the dorsal nucleus of the lateral lemniscus and the superior olivary complex

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.

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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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Dopamine in Auditory Nuclei and Lemniscal Projections is Poised to Influence Acoustic Integration in the Inferior Colliculus

Frontiers in Neural Circuits ◽

10.3389/fncir.2021.624563 ◽

2021 ◽

Vol 15 ◽

Author(s):

Sharonda Harris ◽

Renee Afram ◽

Takashi Shimano ◽

Bozena Fyk-Kolodziej ◽

Paul D. Walker ◽

...

Keyword(s):

Tyrosine Hydroxylase ◽

Inferior Colliculus ◽

Auditory Pathway ◽

Superior Olivary Complex ◽

Lateral Lemniscus ◽

Adult Rats ◽

Dorsal Nucleus ◽

Key Enzyme ◽

6 Hydroxydopamine ◽

Ventral Nucleus

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.

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