Microcircuits of the Ventral Cochlear Nucleus

Rubio, María E.

doi:10.1007/978-3-319-71798-2_3

Cited by 8 publications

(7 citation statements)

References 152 publications

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“…It is unknown whether this requirement is cell-type specific. The VCN contains heterogeneous cell populations including bushy cell (globular and spherical bushy) and stellate cell (D-stellate and T-stellate) ( Oertel, 1991 ; Rubio, 2018 ). They are similarly innervated by the auditory nerve and other synaptic inputs, but with differential physiological properties and ascending projection targets ( Friauf and Ostwald, 1988 ; Cant and Benson, 2003 ; Campagnola and Manis, 2014 ; Heeringa et al, 2018 ; Rubio, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

Peripheral Fragile X messenger ribonucleoprotein is required for the timely closure of a critical period for neuronal susceptibility in the ventral cochlear nucleus

Yu,

Wang

2023

Front. Cell. Neurosci.

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Alterations in neuronal plasticity and critical periods are common across neurodevelopmental diseases, including Fragile X syndrome (FXS), the leading single-gene cause of autism. Characterized with sensory dysfunction, FXS is the result of gene silencing of Fragile X messenger ribonucleoprotein 1 (FMR1) and loss of its product, Fragile X messenger ribonucleoprotein (FMRP). The mechanisms underlying altered critical period and sensory dysfunction in FXS are obscure. Here, we performed genetic and surgical deprivation of peripheral auditory inputs in wildtype and Fmr1 knockout (KO) mice across ages and investigated the effects of global FMRP loss on deafferentation-induced neuronal changes in the ventral cochlear nucleus (VCN) and auditory brainstem responses. The degree of neuronal cell loss during the critical period was unchanged in Fmr1 KO mice. However, the closure of the critical period was delayed. Importantly, this delay was temporally coincidental with reduced hearing sensitivity, implying an association with sensory inputs. Functional analyses further identified early-onset and long-lasting alterations in signal transmission from the spiral ganglion to the VCN, suggesting a peripheral site of FMRP action. Finally, we generated conditional Fmr1 KO (cKO) mice with selective deletion of FMRP in spiral ganglion but not VCN neurons. cKO mice recapitulated the delay in the VCN critical period closure in Fmr1 KO mice, confirming an involvement of cochlear FMRP in shaping the temporal features of neuronal critical periods in the brain. Together, these results identify a novel peripheral mechanism of neurodevelopmental pathogenesis.

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Section: Discussionmentioning

confidence: 99%

Peripheral Fragile X messenger ribonucleoprotein is required for the timely closure of a critical period for neuronal susceptibility in the ventral cochlear nucleus

Yu,

Wang

2023

Front. Cell. Neurosci.

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“…Functionally, electrical coupling between bushy cells in the AVCN might underlie the enhanced temporal synchronization of AVCN output (Rubio 2018), particularly for comparing the timing of spikes in different, closely spaced frequency channels (Rosenberger et al 2003; Covey and Casseday 1999; Covey 2005; Curti et al 2012; Pereda 2014; Rubio and Nagy 2015; Nagy et al 2019). This could be the early auditory computational basis for accurately detecting coincident inputs, which is essential for two features of echolocation: 1) harmonic component analysis and 2) echo delay processing (Simmons et al 2003; Bates and Simmons 2011; Simmons 2014; Finneran et al 2020).…”

Section: Discussionmentioning

confidence: 99%

“…The mammalian cochlear nucleus (CN) receives direct synaptic input from the auditory (8th) cranial nerve. Bushy cells in the ventral cochlear nucleus [VCN, comprising the anteroventral (AVCN) and the anterior portion of the posteroventral (PVCN) cochlear nuclei] exhibit more precise synchronization to the envelope of sounds than do auditory nerve fibers, and convey this temporal information to other brainstem auditory nuclei (Joris and Smith 2008; Rubio 2018). Cells in the dorsal cochlear nucleus (DCN) receive auditory (VCN, auditory nerve) and multimodal input, providing information for localization of sounds in elevation and for head and ear position (Trussell and Oertel 2018).…”

Section: Introductionmentioning

confidence: 99%

Connexin36 expression in the cochlear nucleus complex of the echolocating bat, Eptesicus fuscus

Accomando

Johnson

McLaughlin

et al. 2022

Preprint

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Gap junctions and electrical synapses in the central nervous system are associated with rapid temporal processing and coincidence detection. Using histology, immunohistochemistry, and in situ hybridization, we investigated the distribution of Connexin36 (Cx36), a protein that comprises neuronal gap junctions, throughout the cochlear nucleus complex of the echolocating big brown bat, Eptesicus fuscus, a species exhibiting extreme behavioral sensitivity to minute temporal changes in ultrasonic echoes. For comparison, we visualized Cx36 expression in the cochlear nucleus of transgenic Cx36 reporter mice, species that hear ultrasound but do not echolocate. We observed Cx36 expression in the anteroventral and dorsal cochlear nucleus, with more limited expression in the posteroventral cochlear nucleus, of both species. Several different morphological cell types were labeled, including globular and spherical bushy, octopus, stellate, and fusiform cells. Labeled Cx36 puncta were also observed. Cx36 expression in the bat was spread throughout a relatively smaller area of the cochlear nucleus than in the mouse, even though the bat cochlear nucleus is hypertrophied. In the bat, the anteroventral cochlear nucleus showed higher percent area label than the dorsal cochlear nucleus, with a trend towards the opposite result in the mouse. The presence of gap junctions appears to be a conserved feature of the mammalian cochlear nucleus and thus not uniquely tied to the temporal hyperacuity of echolocation.

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“…These glutamatergic projections are organized anatomically and functionally into distinct sub-nuclei onto at least six different types of principal cell (Brawer et al 1974;Muniak et al 2016). For example, in circuits specialized for temporal encoding in the ipsilateral anteroventral cochlear nucleus (AVCN), ANFs terminate onto somata of bushy cells via large axo-somatic synapses (endbulbs of Held) containing several hundred release sites per terminal (Xu-Friedman & Regehr, 2004;Moser and Strenzke, 2015;Wichmann, 2015;Rubio, 2018). Therefore, in each mammalian ANF, where spike timing is determined by activity at a single ribbon synapse, the timing of each spike may determine the timing of transmitter release at thousands of release sites or active zones (AZs) in the cochlear nucleus.…”

Section: Introductionmentioning

confidence: 99%

Encoding sound in the cochlea: from receptor potential to afferent discharge

Rutherford

Gersdorff

Goutman

2021

The Journal of Physiology

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Ribbon‐class synapses in the ear achieve analog to digital transformation of a continuously graded membrane potential to all‐or‐none spikes. In mammals, several auditory nerve fibres (ANFs) carry information from each inner hair cell (IHC) to the brain in parallel. Heterogeneity of transmission among synapses contributes to the diversity of ANF sound‐response properties. In addition to the place code for sound frequency and the rate code for sound level, there is also a temporal code. In series with cochlear amplification and frequency tuning, neural representation of temporal cues over a broad range of sound levels enables auditory comprehension in noisy multi‐speaker settings. The IHC membrane time constant introduces a low‐pass filter that attenuates fluctuations of the receptor potential above 1–2 kHz. The ANF spike generator adds a high‐pass filter via its depolarization‐rate threshold that rejects slow changes in the postsynaptic potential and its phasic response property that ensures one spike per depolarization. Synaptic transmission involves several stochastic subcellular processes between IHC depolarization and ANF spike generation, introducing delay and jitter that limits the speed and precision of spike timing. ANFs spike at a preferred phase of periodic sounds in a process called phase‐locking that is limited to frequencies below a few kilohertz by both the IHC receptor potential and the jitter in synaptic transmission. During phase‐locking to periodic sounds of increasing intensity, faster and facilitated activation of synaptic transmission and spike generation may be offset by presynaptic depletion of synaptic vesicles, resulting in relatively small changes in response phase. Here we review encoding of spike‐timing at cochlear ribbon synapses.

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Microcircuits of the Ventral Cochlear Nucleus

Cited by 8 publications

References 152 publications

Peripheral Fragile X messenger ribonucleoprotein is required for the timely closure of a critical period for neuronal susceptibility in the ventral cochlear nucleus

Peripheral Fragile X messenger ribonucleoprotein is required for the timely closure of a critical period for neuronal susceptibility in the ventral cochlear nucleus

Connexin36 expression in the cochlear nucleus complex of the echolocating bat, Eptesicus fuscus

Encoding sound in the cochlea: from receptor potential to afferent discharge

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