Long‐term interaction between microglial cells and cochlear nucleus neurons after bilateral cochlear ablation

Fuentes–Santamaría, Verónica; Alvarado, Juan Carlos; Juı́z, José M.

doi:10.1002/cne.23088

Cited by 29 publications

(60 citation statements)

References 95 publications

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“…An increase in astrocytes was found in chick brainstem after CR in n. magnocellularis , the avian homolog of the anteroventral cochlear nucleus (Rubel and MacDonald, 1992, Lurie and Rubel, 1994). Prior studies in mammals have also shown that both microglia and astrocytes are upregulated in the cochlear nucleus in response to unilateral inner ear lesions in adult rats (de Waele et al, 1996, Campos Torres et al, 1999, Campos-Torres et al, 2005, Fuentes-Santamaria et al, 2012). These studies showed changes in the cochlear nucleus, the primary target denervated by CR.…”

Section: Discussionmentioning

confidence: 87%

Distribution of glial cells in the auditory brainstem: Normal development and effects of unilateral lesion

et al. 2014

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Auditory brainstem networks facilitate sound source localization through binaural integration. A key component of this circuitry is the projection from the ventral cochlear nucleus (VCN) to the medial nucleus of the trapezoid body (MNTB), a relay nucleus that provides inhibition to the superior olivary complex. This strictly contralateral projection terminates in the large calyx of Held synapse. The formation of this pathway requires spatiotemporal coordination of cues that promote cell maturation, axon growth, and synaptogenesis. Here we have examined the emergence of distinct classes of glial cells, which are known to function in development and in response to injury. Immunofluorescence for several astrocyte markers revealed unique expression patterns. ALDH1L1 was expressed earliest in both nuclei, followed by S100β, during the first postnatal week. GFAP expression was seen in the second postnatal week. GFAP-positive cell bodies remained outside the boundaries of VCN and MNTB, with a limited number of labeled fibers penetrating into the margins of the nuclei. OLIG2 expression revealed the presence of oligodendrocytes in VCN and MNTB from birth until after hearing onset. In addition, IBA1-positive microglia were observed after the first postnatal week. Following hearing onset, all glial populations were found in MNTB. We then determined the distribution of glial cells following early (P2) unilateral cochlear removal, which results in formation of ectopic projections from the intact VCN to ipsilateral MNTB. We found that following perturbation, astrocytic markers showed expression near the ectopic ipsilateral calyx. Taken together, the developmental expression patterns are consistent with a role for glial cells in the maturation of the calyx of Held and suggest that these cells may have a similar role in maturation of lesion-induced connections.

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Section: Discussionmentioning

confidence: 87%

Distribution of glial cells in the auditory brainstem: Normal development and effects of unilateral lesion

et al. 2014

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“…Janz and Illing (2014) found activated microglia in cochlear nuclei as early as one day after cochlear ablation. Fuentes-Santamaria et al (2012) found changes in the relative positions of activated microglia and neurons at 100 days postablation and suggested that the function of these activated microglia was to facilitate changes in neuronal function. Thus the time courses of changes in the cochlea and auditory brainstem following cochlear ablation and noise trauma are very different, and may be mediated by different mechanisms (as suggested by Morest et al, 1998); activated microglia may have different roles in the two paradigms.…”

Section: Discussionmentioning

confidence: 98%

“…The suggestion that activated microglia might participate in auditory plasticity came from studies of a different model of auditory plasticity, cochlear ablation (Campos Torres et al, 1999, Fuentes-Santamaria et al, 2012, Janz and Illing, 2014). Both auditory nerve degeneration and brainstem plasticity occur much more rapidly after cochlear ablations than after acoustic trauma.…”

Section: Discussionmentioning

confidence: 99%

“…At present, little is known about the role of microglia in noise trauma-induced changes in the CN. Several studies have described activated microglia in the CN after cochlear lesions (Campos Torres et al, 1999, Fuentes-Santamaria et al, 2012, Janz and Illing, 2014) and proposed a role for activated microglia in CN plasticity. However, it is possible that the activated microglia were simply serving their traditional role as scavengers (Kreutzberg, 1996), removing the debris from auditory nerve degeneration.…”

Section: Introductionmentioning

confidence: 99%

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Effects of acoustic trauma on the auditory system of the rat: The role of microglia

Baizer

Wong

Manohar³

et al. 2015

Neuroscience

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Exposure to loud, prolonged sounds (acoustic trauma, AT) leads to the death of both inner and outer hair cells (IHCs and OHCs), death of neurons of the spiral ganglion and degeneration of the auditory nerve. The auditory nerve (8cn) projects to the three subdivisions of the cochlear nuclei (CN), the dorsal cochlear nucleus (DC) and the anterior (VCA) and posterior (VCP) subdivisions of the ventral cochlear nucleus. There is both anatomical and physiological evidence for plastic reorganization in the denervated CN after AT. Anatomical findings show axonal sprouting and synaptogenesis; physiologically there is an increase in spontaneous activity suggesting reorganization of circuitry. The mechanisms underlying this plasticity are not understood. Recent data suggest that activated microglia may have a role in facilitating plastic reorganization in addition to removing trauma-induced debris. In order to investigate the roles of activated microglia in the CN subsequent to acoustic trauma we exposed animals to bilateral noise sufficient to cause massive hair cell death. We studied four groups of animals at different survival times: 30 days, 60 days, 6 months and 9 months. We used silver staining to examine the time course and pattern of auditory nerve degeneration, and immunohistochemistry to label activated microglia in the denervated CN. We found both degenerating auditory nerve fibers and activated microglia in the CN at 30 and 60 days and 6 months after AT. There was close geographic overlap between the degenerating fibers and activated microglia, consistent with a scavenger role for activated microglia. At the longest survival time, there were still silver-stained fibers but very little staining of activated microglia in overlapping regions. There were, however, activated microglia in the surrounding brainstem and cerebellar white matter.

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“…As in the cochlear nucleus regions, glutamine and taurine levels increased in most lesioned-side vestibular nuclear regions as compared to contralateral. Since these two amino acids tend to be more concentrated in glia than in neurons (Patel and Hunt, 1985; Ottersen et al, 1992; Hassel et al, 1995), their increases may be related to the gliosis reported in both cochlear and vestibular nuclei after inner ear lesions (Campos Torres et al, 1999; Li et al, 1999; Fuentes-Santamaría et al, 2012). On the other hand, the increases in glutamine and taurine levels after the peripheral lesion were generally less striking in vestibular nuclei than in the cochlear nucleus, as were any changes in the levels of the other amino acids less closely related to synaptic transmission.…”

Section: Discussionmentioning

confidence: 99%

Effects of cochlear ablation on amino acid levels in the rat cochlear nucleus and superior olive

Godfrey¹,

Jin²,

Liu³

et al. 2014

Hearing Research

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Amino acids have important roles in the chemistry of the auditory system, including communication among neurons. There is much evidence for glutamate as a neurotransmitter from auditory nerve fibers to cochlear nucleus neurons. Previous studies in rodents have examined effects of removal of auditory nerve input by cochlear ablation on levels, uptake and release of glutamate in cochlear nucleus subdivisions, as well as on glutamate receptors. Effects have also been reported on uptake and release of γ-aminobutyrate (GABA) and glycine, two other amino acids strongly implicated in cochlear nucleus synaptic transmission. We mapped the effects of cochlear ablation on the levels of amino acids, including glutamate, GABA, glycine, aspartate, glutamine, taurine, serine, threonine, and arginine, in microscopic subregions of the rat cochlear nucleus. Submicrogram-size samples microdissected from freeze-dried brainstem sections were assayed for amino acid levels by high performance liquid chromatography. After cochlear ablation, glutamate and aspartate levels decreased by 2 days in regions receiving relatively dense innervation from the auditory nerve, whereas the levels of most other amino acids increased. The results are consistent with a close association of glutamate and aspartate with auditory nerve fibers and of other amino acids with other neurons and glia in the cochlear nucleus. A consistent decrease of GABA level in the lateral superior olive could be consistent with a role in some lateral olivocochlear neurons. The results are compared with those obtained with the same methods for the rat vestibular nerve root and nuclei after vestibular ganglionectomy.

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Long‐term interaction between microglial cells and cochlear nucleus neurons after bilateral cochlear ablation

Cited by 29 publications

References 95 publications

Distribution of glial cells in the auditory brainstem: Normal development and effects of unilateral lesion

Distribution of glial cells in the auditory brainstem: Normal development and effects of unilateral lesion

Effects of acoustic trauma on the auditory system of the rat: The role of microglia

Effects of cochlear ablation on amino acid levels in the rat cochlear nucleus and superior olive

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