scholarly journals Trigeminal Contributions to the Dorsal Cochlear Nucleus in Mouse

2021 ◽  
Vol 15 ◽  
Author(s):  
Timothy S. Balmer ◽  
Laurence O. Trussell
Keyword(s):  
Cochlear Nucleus ◽  
Granule Cells ◽  
Auditory Pathway ◽  
Dorsal Cochlear Nucleus ◽  
Auditory Information ◽  
Sound Sources ◽  
Brush Cells ◽  
Important Species ◽  
Axonal Projections ◽  
Auditory Signals

The dorsal cochlear nucleus (DCN) is the first site of multisensory integration in the auditory pathway of mammals. The DCN circuit integrates non-auditory information, such as head and ear position, with auditory signals, and this convergence may contribute to the ability to localize sound sources or to suppress perceptions of self-generated sounds. Several extrinsic sources of these non-auditory signals have been described in various species, and among these are first- and second-order trigeminal axonal projections. Trigeminal sensory signals from the face and ears could provide the non-auditory information that the DCN requires for its role in sound source localization and cancelation of self-generated sounds, for example, head and ear position or mouth movements that could predict the production of chewing or licking sounds. There is evidence for these axonal projections in guinea pigs and rats, although the size of the pathway is smaller than might be expected for a function essential for a prey animals’ survival. However, evidence for these projections in mice, an increasingly important species in auditory neuroscience, is lacking, raising questions about the universality of such proposed functions. We therefore investigated the presence of trigeminal projections to the DCN in mice, using viral and transgenic approaches. We found that the spinal trigeminal nucleus indeed projects to DCN, targeting granule cells and unipolar brush cells. However, direct axonal projections from the trigeminal ganglion itself were undetectable. Thus, secondary brainstem sources carry non-auditory signals to the DCN in mice that could provide a processed trigeminal signal to the DCN, but primary trigeminal afferents are not integrated directly by DCN.

scholarly journals Molecular Layer Inhibitory Interneurons Provide Feedforward and Lateral Inhibition in the Dorsal Cochlear Nucleus

2010 ◽  
Vol 104 (5) ◽  
pp. 2462-2473 ◽  
Author(s):  
Michael T. Roberts ◽  
Laurence O. Trussell
Keyword(s):  
Brain Stem ◽  
Lateral Inhibition ◽  
Cochlear Nucleus ◽  
Molecular Layer ◽  
Dorsal Cochlear Nucleus ◽  
Inhibitory Input ◽  
Auditory Information ◽  
Parallel Fibers ◽  
Sensory Inputs ◽  
Cartwheel Cells

In the outer layers of the dorsal cochlear nucleus, a cerebellum-like structure in the auditory brain stem, multimodal sensory inputs drive parallel fibers to excite both principal (fusiform) cells and inhibitory cartwheel cells. Cartwheel cells, in turn, inhibit fusiform cells and other cartwheel cells. At the microcircuit level, it is unknown how these circuit components interact to modulate the activity of fusiform cells and thereby shape the processing of auditory information. Using a variety of approaches in mouse brain stem slices, we investigated the synaptic connectivity and synaptic strength among parallel fibers, cartwheel cells, and fusiform cells. In paired recordings of spontaneous and evoked activity, we found little overlap in parallel fiber input to neighboring neurons, and activation of multiple parallel fibers was required to evoke or alter action potential firing in cartwheel and fusiform cells. Thus neighboring neurons likely respond best to distinct subsets of sensory inputs. In contrast, there was significant overlap in inhibitory input to neighboring neurons. In recordings from synaptically coupled pairs, cartwheel cells had a high probability of synapsing onto nearby fusiform cells or other nearby cartwheel cells. Moreover, single cartwheel cells strongly inhibited spontaneous firing in single fusiform cells. These synaptic relationships suggest that the set of parallel fibers activated by a particular sensory stimulus determines whether cartwheel cells provide feedforward or lateral inhibition to their postsynaptic targets.

Vertical Cell Responses to Sound in Cat Dorsal Cochlear Nucleus

1999 ◽  
Vol 82 (2) ◽  
pp. 1019-1032 ◽  
Author(s):  
William S. Rhode
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Molecular Layer ◽  
Broadband Noise ◽  
Dorsal Cochlear Nucleus ◽  
Type Ii ◽  
Fusiform Cell ◽  
Sound Sources ◽  
Tuning Curves ◽  
Axonal Arbors

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds ∼27 dB SPL, spontaneous firing rates of ∼0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.

scholarly journals Synaptic Inputs to Granule Cells of the Dorsal Cochlear Nucleus

2008 ◽  
Vol 99 (1) ◽  
pp. 208-219 ◽  
Author(s):  
Veeramuthu Balakrishnan ◽  
Laurence O. Trussell
Keyword(s):  
Granule Cell ◽  
Cochlear Nucleus ◽  
Granule Cells ◽  
Cerebellar Granule Cells ◽  
Dorsal Cochlear Nucleus ◽  
Excitatory Postsynaptic Currents ◽  
Synaptic Inputs ◽  
Postsynaptic Currents ◽  
Cell Circuit

The mammalian dorsal cochlear nucleus (DCN) integrates auditory nerve input with nonauditory signals via a cerebellar-like granule cell circuit. Although granule cells carry nonauditory information to the DCN, almost nothing is known about their physiology. Here we describe electrophysiological features of synaptic inputs to granule cells in the DCN by in vitro patch-clamp recordings from P12 to P22 rats. Granule cells ranged from 6 to 8 μm in cell body diameter and had high-input resistance. Excitatory postsynaptic currents consisted of both AMPA receptor-mediated and N-methyl-d-aspartate receptor-mediated currents. Synaptically evoked excitatory postsynaptic currents ranged from −25 to −140 pA with fast decay time constants. Synaptic stimulation evoked both short- and long-latency synaptic responses that summated to spike threshold, indicating the presence of a polysynaptic excitatory pathway in the granule cell circuit. Synaptically evoked inhibitory postsynaptic currents in Cl−-loaded cells ranged from −30 to −1,021 pA and were mediated by glycine and, to a lesser extent, GABAA receptors. Unlike cerebellar granule cells, DCN granule cells lacked tonic inhibition by GABA. The glycinergic synaptic conductance was mediated by heteromeric glycine receptors and was far stronger than the glutamatergic conductance, suggesting that glycinergic neurons may act to gate nonauditory signals in the DCN.

scholarly journals Alleviation of Tinnitus With High-Frequency Stimulation of the Dorsal Cochlear Nucleus: A Rodent Study

2019 ◽  
Vol 23 ◽  
pp. 233121651983508 ◽  
Author(s):  
Gusta van Zwieten ◽  
Ali Jahanshahi ◽  
Marlieke L. van Erp ◽  
Yasin Temel ◽  
Robert J. Stokroos ◽  
...  
Keyword(s):  
Neuronal Activity ◽  
Cochlear Nucleus ◽  
High Frequency ◽  
Auditory Pathway ◽  
Dorsal Cochlear Nucleus ◽  
High Frequency Stimulation ◽  
Noise Trauma ◽  
Frequency Stimulation ◽  
Central Auditory Pathway ◽  
Stimulation Of

Deep brain stimulation of the central auditory pathway is emerging as a promising treatment modality for tinnitus. Within this pathway, the dorsal cochlear nucleus (DCN) plays a key role in the pathophysiology of tinnitus and is believed to be a tinnitus generator. We hypothesized that high-frequency stimulation (HFS) of the DCN would influence tinnitus-related abnormal neuronal activity within the auditory pathway and hereby suppress tinnitus. To this end, we assessed the effect of HFS of the DCN in a noise-induced rat model of tinnitus. The presence of tinnitus was verified using the gap prepulse inhibition of the acoustic startle response paradigm. Hearing thresholds were determined before and after noise trauma by measuring the auditory brainstem responses. In addition, changes in neuronal activity induced by noise trauma and HFS were assessed using c-Fos immunohistochemistry in related structures. Results showed tinnitus development after noise trauma and hearing loss ipsilateral to the side exposed to noise trauma. During HFS of the DCN, tinnitus was suppressed. There was no change in c-Fos expression within the central auditory pathway after HFS. These findings suggest that DCN-HFS changes patterns of activity and results in information lesioning within the network and hereby blocking the relay of abnormal tinnitus-related neuronal activity.

scholarly journals Stimulus-timing-dependent modifications of rate-level functions in animals with and without tinnitus

2015 ◽  
Vol 113 (3) ◽  
pp. 956-970 ◽  
Author(s):  
Roxana A. Stefanescu ◽  
Seth D. Koehler ◽  
Susan E. Shore
Keyword(s):  
Cochlear Nucleus ◽  
Hebbian Learning ◽  
Auditory Pathway ◽  
Dorsal Cochlear Nucleus ◽  
Firing Rates ◽  
Bimodal Stimulation ◽  
Rate Level ◽  
Learning Rules ◽  
Stimulus Timing

Tinnitus has been associated with enhanced central gain manifested by increased spontaneous activity and sound-evoked firing rates of principal neurons at various stations of the auditory pathway. Yet, the mechanisms leading to these modifications are not well understood. In a recent in vivo study, we demonstrated that stimulus-timing-dependent bimodal plasticity mediates modifications of spontaneous and tone-evoked responses of fusiform cells in the dorsal cochlear nucleus (DCN) of the guinea pig. Fusiform cells from sham animals showed primarily Hebbian learning rules while noise-exposed animals showed primarily anti-Hebbian rules, with broadened profiles for the animals with behaviorally verified tinnitus (Koehler SD, Shore SE. J Neurosci 33: 19647–19656, 2013a). In the present study we show that well-timed bimodal stimulation induces alterations in the rate-level functions (RLFs) of fusiform cells. The RLF gains and maximum amplitudes show Hebbian modifications in sham and no-tinnitus animals but anti-Hebbian modifications in noise-exposed animals with evidence for tinnitus. These findings suggest that stimulus-timing bimodal plasticity produced by the DCN circuitry is a contributing mechanism to enhanced central gain associated with tinnitus.

Temporal and Frequency Characteristics of Cartwheel Cells in the Dorsal Cochlear Nucleus of the Awake Mouse

2007 ◽  
Vol 98 (2) ◽  
pp. 744-756 ◽  
Author(s):  
Christine V. Portfors ◽  
Patrick D. Roberts
Keyword(s):  
Auditory Processing ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Active Role ◽  
Auditory Pathway ◽  
Dorsal Cochlear Nucleus ◽  
Central Auditory Processing ◽  
Complex Frequency ◽  
Principal Cells ◽  
Cartwheel Cells

The dorsal cochlear nucleus (DCN) is an initial site of central auditory processing and also the first site of multisensory convergence in the auditory pathway. The auditory nerve imparts a tonotopic frequency organization on the responses of principal cells in the DCN. Cartwheel cells modify the responses of principal cells, but they do not receive direct auditory nerve input. This study shows that cartwheel cells respond well to tonal stimuli in the awake mouse and they have a well-defined characteristic frequency that corresponds to the tonotopic organization of the DCN. The auditory responses of cartwheel cells exhibit complex spectrotemporal responses to tones, with excitation and inhibition modulating the firing patterns in both frequency and time after onset of the stimulus. Temporal responses to best-frequency tones are highly variable between cartwheel cells, but a simple model is used to unify this variability as differences in the timing of synaptic currents. Cartwheel cell responses to two-tone stimuli show that interactions from different frequencies affect the output of cartwheel cells. The results suggest that at this primary auditory structure, processing of sound at one frequency can be modified by sounds of different frequency. These complex frequency and temporal interactions in cartwheel cells suggest that these neurons play an active role in basic sound processing.

In Vitro Studies of Neuromodulation and Plasticity in the Dorsal Cochlear Nucleus

2018 ◽  
pp. 122-142 ◽  
Author(s):  
Laurence O. Trussell
Keyword(s):  
Synaptic Plasticity ◽  
Auditory Processing ◽  
Cochlear Nucleus ◽  
Cell Types ◽  
Auditory Pathway ◽  
Dorsal Cochlear Nucleus ◽  
Membrane Properties ◽  
Auditory Input ◽  
Dynamic Tuning

The dorsal cochlear nucleus (DCN), a division of the cochlear nuclear complex, has been the subject of intense interest for its role in auditory processing and hearing disorders. The tonotopic layout of DCN principal cells and the refinement of processing of auditory signals by interneurons are together thought to permit encoding of sound source elevation. However, the many cell types and complex connectivity of the DCN suggest more diverse functions than localization. A prominent non-auditory input to the DCN has been proposed to assist in such functions as orienting to sounds of interest, detecting moving sounds, or cancelling self-generated sounds. Synaptic plasticity in the DCN may be essential for dynamic tuning of non-auditory input. Indeed, long-term changes in synaptic or membrane properties could underlie tinnitus, which is associated with hyperactivity in the DCN in some animal models. Finally, the DCN is invested with wide-ranging neuromodulatory mechanisms, suggesting that changes in the behavioral state of animals associated with such neuromodulatory systems might alter sensory processing at the earliest stages of the auditory pathway. This review will focus on studies that have utilized the in vitro brain slice approach to identify basic mechanisms of synaptic plasticity and neuromodulation in the DCN.

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