Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil

Kil, Jonathan; Hkageyama, Glenn; Semple, Malcolm N.; Kitzes, L. M.

doi:10.1002/cne.903530302

Cited by 85 publications

(90 citation statements)

References 75 publications

(91 reference statements)

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“…Young calyces appear to grow unidirectionally from their point of contact onto the MNTB cell (Ramó n y Cajal, 1909;Morest, 1968b;Kandler and Friauf, 1993;Kil et al, 1995). Our data show that late-stage protocalyx and young calyx geometry consists of a cup-shaped area with branch-like edges that can form small collateral inputs onto another cell (Fig.…”

Section: Directed Growth Of the Calyx Of Heldmentioning

confidence: 65%

“…7). These calycine collaterals have been well documented (Morest, 1968b;Kandler and Friauf, 1993;Kil et al, 1995) and may represent a second stage of multi-innervation that follows young calyx formation. These small collaterals do not appear capable of generating calyxlike synaptic currents and, as mentioned previously, only persist into adulthood as fine branches Kuwabara et al, 1991;Smith et al, 1991;Kandler and Friauf, 1993).…”

Section: Directed Growth Of the Calyx Of Heldmentioning

confidence: 84%

“…These processes (Fig. 2, blue) could be thin axons or growth cone processes and may originate from the cochlear nucleus (Kil et al, 1995); they could not be traced to their origin within the set of serial sections. A closer examination of functional contacts reveals both synapses (Fig.…”

Section: Structural Development Mirrors Physiological Observations Vementioning

confidence: 99%

“…The stages of calyx formation have been described in pioneering light-microscopic studies (Morest, 1968b;Kandler and Friauf, 1993;Kil et al, 1995). As described originally in the opossum, a growth cone expands into a protocalyx then further enlarges into a cup-shaped structure, the young calyx, that envelops ϳ50% of the postsynaptic cell body (Morest, 1968b;Satzler et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…The incidence of multi-innervation revealed by these studies was small but considered to be minimal estimates of a more prevalent phenomenon for pruning supernumerary calyces as they mature into their adult form. As early as P0, nerve terminals that originate from the cochlear nucleus form synaptic contacts, revealed using electron microscopy, onto MNTB neurons (Kil et al, 1995). We undertook systematic functional and ultrastructural examinations across early postnatal ages to pinpoint when increases in synaptic currents and the number of contacts associated with formation of the protocalyx occur, and to quantify protocalyx growth into a young calyx.…”

Section: Introductionmentioning

confidence: 99%

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Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation

Hoffpauir

Grimes²,

Mathers³

et al. 2006

J. Neurosci.

114

229

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Synaptogenesis during early development is thought to follow a canonical program whereby synapses increase rapidly in number and individual axons multiply-innervate nearby targets. Typically, a subset of inputs then out-competes all others through experience-driven processes to establish stable, long-lasting contacts. We investigated the formation of the calyx of Held, probably the largest nerve terminal in the mammalian CNS. Many basic functional and morphological features of calyx growth have not been studied previously, including whether mono-innervation, a hallmark of this system in adult animals, is established early in development. Evoked postsynaptic currents, recorded from neonatal mice between postnatal day 1 (P1) and P4, increased dramatically from Ϫ0.14 Ϯ 0.04 nA at P1 to Ϫ6.71 Ϯ 0.65 nA at P4 with sharp jumps between P2 and P4. These are the first functional assays of these nascent synapses for ages less than P3. AMPA and NMDA receptor-mediated currents were prominent across this age range. Electron microscopy (EM) revealed a concomitant increase, beginning at P2, in the prevalence of postsynaptic densities (16-fold) and adhering contacts (73-fold) by P4. Therefore, both functional and structural data showed that young calyces could form within 2 d, well before the onset of hearing around P8. Convergence of developing calyces onto postsynaptic targets, indicative of competitive processes that precede mono-innervation, was rare (4 of 29) at P4 as assessed using minimal stimulation electrophysiology protocols. Serial EM sectioning through 19 P4 cells further established the paucity (2 of 19) of convergence. These data indicate that calyces of Held follow a noncanonical program to establish targeted innervation that occurs over a rapid time course and precedes auditory experience.

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Section: Directed Growth Of the Calyx Of Heldmentioning

confidence: 65%

Section: Directed Growth Of the Calyx Of Heldmentioning

confidence: 84%

Section: Structural Development Mirrors Physiological Observations Vementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation

Hoffpauir

Grimes²,

Mathers³

et al. 2006

J. Neurosci.

114

229

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Regional distribution of neurotrophin receptors in the developing auditory brainstem

1996

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Neuron survival and axonal regeneration become severely limited during early postnatal development. In conjunction with our recent organotypic analysis of regeneration in the auditory midbrain, we wished to determine whether neurotrophins could serve as a trophic substance during the postnatal period. Therefore, the current study examines the development of three neurotrophin receptor tyrosine kinases (TrkA, TrkB, and TrkC) in the gerbil auditory brainstem. Immunoreactivity to TrkA, the nerve growth-factor receptor, was observed in nonneuronal cells during the first two postnatal weeks. In the cochlear nucleus of mature animals, however, there was a TrkA-positive neuronal subpopulation. In contrast, immunoreactivity to TrkB and TrkC (the receptors for brain-derived neurotrophic factor and neurotrophin-3, respectively) displayed a widespread distribution in the auditory brainstem. At postnatal day 0, TrkB and TrkC staining was virtually absent from auditory nuclei, although immunopositive neurons were present in the mesencephalic trigeminal nucleus. By postnatal day 7, TrkB- and TrkC-positive neurons were present in most brainstem auditory nuclei. At postnatal day 15, TrkB immunoreactivity was observed throughout the inferior colliculus (IC), the cochlear nucleus, the medial and lateral nuclei of the trapezoid body, and the lateral superior olive, whereas TrkC labeled only a subpopulation of neurons within the central nucleus of the IC. The TrkB immunoreactivity was present on both neuronal somata and dendrites, whereas TrkC was generally restricted to cell bodies. At postnatal day 30, TrkB immunostaining was observed on most neurons of the IC. The medial and lateral nuclei of the trapezoid body displayed extremely strong TrkB staining, followed by the cochlear nucleus. In contrast, the TrkC immunostaining was decreased dramatically by postnatal day 21. Observations at the ultrastructural level confirmed a neuronal localization of TrkB and TrkC. Immunostaining for both receptors was restricted largely to the postsynaptic density of synaptic profiles in both dendrites and somata. In summary, this study illustrates a differential pattern of immunoreactivity between three neurotrophin receptors during development. The general increase of TrkB expression is well correlated with the onset of sound-evoked activity in this system, and its synaptic localization suggests that it may be involved in the modulation or maintenance of postsynaptic physiology.

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Susceptibility of developing cochlear nucleus neurons to deafferentation-induced death abruptly ends just before the onset of hearing

Tierney¹,

Russell²,

Moore³

1997

J. Comp. Neurol.

157

101

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To investigate the ability of developing cochlear nucleus (CN) neurons to survive in the absence of afferent input, left cochlear removals were performed on gerbils at 2 day intervals from postnatal (P)3 to P11, and at P18 and P93. After a 3 month postsurgical survival period, Nissl-stained frontal sections through the brainstem were analyzed under the light microscope. CN volume, anteroventral cochlear nucleus (AVCN) neuron cross-sectional area, and total number of neurons in the CN were measured on both sides of the brain. Mean volume reduction of the deafferented CN relative to the intact CN ranged between 76% in the P3 group to 33% in the P11 group and did not differ significantly between P11 and P93. Cochlear removal at all ages reduced AVCN neuron cross-sectional area by approximately 40% in the deafferented CN relative to the intact CN, except for the P93 group where neuron atrophy was significantly less severe (23% mean reduction). Massive loss of CN neurons (>50% of the intact side) was observed following cochlear removal performed during the first postnatal week. However, between P7 and P9, neurons in all areas of the CN lose susceptibility to deafferentation-induced neuron death. No significant neuron loss was observed following cochlear removal after P7. This study shows that an abrupt transition in the ability of CN neurons to survive in the absence of afferent input is coincident with events leading to the onset of hearing.

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Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil

Cited by 85 publications

References 75 publications

Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation

Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation

Regional distribution of neurotrophin receptors in the developing auditory brainstem

Susceptibility of developing cochlear nucleus neurons to deafferentation-induced death abruptly ends just before the onset of hearing

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