Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei

Zhou, Ning; Taylor, Dwan A.; Parks, Thomas N.

doi:10.1097/00001756-199511270-00002

Cited by 48 publications

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“…It is possible that CNQX and NBQX block some interaction of ambient glutamate (Haberecht and Redburn, 1996) with AMPA /kainate receptors on NM and NL neurons before the formation of functioning synapses. At least in NM, such a mechanism could not involve calcium-permeable non-NMDA receptors, however, because they do not appear until after E11 (Zhou et al, 1995). In view of this, we now favor the hypothesis that CNQX and NBQX increase production of one or more diffusible factors that act on auditory neurons to promote their survival.…”

Section: Discussionmentioning

confidence: 87%

“…For these reasons, NM and NL have been used extensively in studies of the control of neuron survival by afferent synaptic connections and activity (Rubel and Parks, 1988;Rubel et al, 1990). Calcium-permeable AMPA receptors are prominently expressed in NM and NL during development (Zhou et al, 1995) and mediate normal synaptic transmission (Otis et al, 1995). Normal programmed cell death in NL occurs during a period when these neurons receive rhythmic spontaneous excitation via afferent pathways originating in the cochlea and acting via AMPA receptors (Lippe, 1994).…”

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confidence: 99%

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Prevention of Normally Occurring and Deafferentation-Induced Neuronal Death in Chick Brainstem Auditory Neurons by Periodic Blockade of AMPA/Kainate Receptors

Solum

Hughes

et al. 1997

J. Neurosci.

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The role of glutamate receptors in regulating programmed neuronal death and deafferentation-induced neuronal death in the brainstem auditory nuclei was studied by in ovo drug administration to chick embryos. The nucleus laminaris (NL) undergoes programmed developmental cell death of 19% between embryonic day 9 (E9) and E17. The AMPA/kainate receptor antagonist CNQX, when administered at doses of 200 -300 g/d from E8 to E15, prevented programmed neuronal death in NL through at least posthatching day 8, without producing anatomical or behavioral abnormalities. 3-((RS)Ϫ2-Carboxypiperazin-4-yl)-propyl-1-phosphonic acid, an antagonist of NMDA receptors, had no effect on normal cell death in the NL. CNQX, given from E8 to E15 or only from E8 to E10, also blocked the 33% neuronal loss in the nucleus magnocellularis (NM) that follows surgical destruction of the otocyst on E3, a procedure that deafferents NM neurons by preventing formation of the cochlear nerve. Treatment either with CNQX or the more highly selective NBQX from E8 to E10, before the onset of synaptic transmission in NM and NL, was also effective in preventing normal neuronal death in NL. Analysis of the effects of CNQX or NBQX on spontaneous embryonic motility at E10 showed that the doses effective in preventing neuronal death suppressed motility for Ͻ8 hr. We conclude that periodic blockade of AMPA/kainate receptors can protect CNS neurons against subsequent programmed cell death or deafferentation-induced death. Key words: neuroprotection; glutamate; programmed cell death; apoptosis; auditory system; cochlear nuclei; CNQX; NBQX; CPP; nucleus laminaris; nucleus magnocellularisModulation of glutamate receptor function can have profound effects on developing neurons. These effects, which are thought to depend on receptor-mediated changes in cytosolic calcium concentration, include changes in neurite outgrowth, synapse formation, expression of neurotrophins and their receptors, expression of the glutamate receptor, and neuronal survival (Mattson, 1996). Because the NMDA subtype of the glutamate receptor is prominent in many CNS regions during key periods in development and is a major source of calcium influx in many neurons (Mori and Mishina, 1995), the role of this receptor subtype in nervous system development has received extensive study (Scheetz and Constantine-Paton, 1994). The non-NMDA receptors, however, are the main mediators of excitatory neurotransmission (Collingridge and Lester, 1989;Bettler and Mulle, 1995) and in a number of CNS regions are also permeable to calcium ions (Jonas and Burnashev, 1995). Calcium-permeable AMPA /kainate receptors have been shown to confer susceptibility to excitotoxic death in cultured spinal cord neurons (Carriedo et al., 1996), and normal neuronal death in the chick spinal cord is increased by treatments purported to raise intracellular calcium levels (Ciutat et al., 1994). It is not known, however, whether non-NMDA receptors are important in controlling cell number during development.The present study examined th...

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Section: Discussionmentioning

confidence: 87%

mentioning

confidence: 99%

Prevention of Normally Occurring and Deafferentation-Induced Neuronal Death in Chick Brainstem Auditory Neurons by Periodic Blockade of AMPA/Kainate Receptors

Solum

Hughes

et al. 1997

J. Neurosci.

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“…Lawrence and Trussell (2000) suggested that a reduction in flip expression contributes to the developmental changes in AMPAR kinetics in the chick nMag. Other studies using calcium permeability measurements and molecular analysis suggest a low expression level of the GluR2 subunit in the rat and chick auditory neurons Otis et al, 1995;Zhou et al, 1995;Ravindranathan et al, 2000). This was supported by enhanced spermine sensitivity during early development (Washburn et al, 1997).…”

Section: Mechanisms Underlying Age-dependent Acceleration In Ampar Dementioning

confidence: 82%

“…AMPARs that contain the GluR4 subunit may mediate fast synaptic transmission in rat and chick auditory synapses Otis et al, 1995;Zhou et al, 1995;Caicedo and Eybalin, 1999;Ravindranathan et al, 2000). We postulated that during development, the AMPAR complex might switch from subunits that are slow gating and Ca 2ϩ impermeable to fast-gating Ca 2ϩ permeable compositions (e.g., from GluR2 to GluR4), leading to the accelerated decay time course.…”

Section: Ampars Devoid Of Glur2 Mediate Synaptic Transmission During mentioning

confidence: 99%

“…Auditory synapses are particularly enriched in the fast gating GluR4 flop subunit, and AMPARs at these synapses are often permeable to Ca 2ϩ because of a lack of the GluR2 subunit, which eliminates Ca 2ϩ permeability Otis et al, 1995;Zhou et al, 1995;Caicedo and Eybalin, 1999;Ravindranathan et al, 2000). It is unknown, however, whether Ca 2ϩ permeability is conferred to synaptic AMPARs at the onset of synaptogenesis or a later developmental stage.…”

Section: Introductionmentioning

confidence: 99%

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The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

Joshi¹,

Shokralla²,

Titis³

et al. 2004

J. Neurosci.

102

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During early postnatal development of auditory synapses, the decay time course of AMPA receptor (AMPAR) EPSCs accelerates markedly, but the mechanisms underlying this process remain uncertain. Using the developing calyx of Held synapse in the mouse auditory brainstem, we have examined presynaptic and postsynaptic elements that may regulate decay kinetics of AMPAR EPSCs. We found that the decay time kinetics was voltage dependent in both immature and mature synapses, being slower at positive potentials than negative potentials. By recording evoked miniature events in extracellular Ca 2ϩ or Sr 2ϩ , we revealed a significant decrease in decay time constants of EPSCs as maturation progresses. On the basis of internal and external polyamine block of AMPAR EPSCs and immunohistochemistry assays with subunit-specific antibodies, we demonstrated that the glutamate receptor (GluR) 2 subunit is virtually absent at all developmental ages. Antibody staining patterns suggest a gradual shift in subunit composition from GluR1-to GluR3/4-dominant phenotypes. Kinetic analyses of deactivation, desensitization, and recovery from desensitization in outside-out patches in response to ultrafast application of glutamate lend supportive evidence that such a shift in the gating phenotype likely accounts for the accelerated time course throughout development. Finally, by pharmacologically manipulating AMPAR gating and using simulated EPSCs to evoke action potentials, we demonstrated that rapid decay kinetics of AMPAR EPSCs is essential for this synapse to accommodate high-frequency firing without compromising spike amplitude. Hence, developmental alterations in the subunit composition likely dictate changes in the time course of AMPAR EPSCs and play an indispensable role in the refinement of high-fidelity neurotransmission at the calyx of Held synapse.

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Calretinin expression in the chick brainstem auditory nuclei develops and is maintained independently of cochlear nerve input

Parks

Code²,

Taylor

et al. 1997

J. Comp. Neurol.

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The expression of the calcium-binding protein calretinin (CR) in the chick brainstem auditory nuclei angularis (NA), laminaris (NL), and magnocelularis (NM) was studied during normal development and after deafening by surgical removal of the otocyst (embryonic precursor of the inner ear) or columella (middle ear ossicle). CR mRNA was localized by in situ hybridization by using a radiolabeled oligonucleotide chick CR probe. CR immunoreactivity (CR-IR) was localized on adjacent tissue sections. CR mRNA signal in the auditory nuclei was expressed at comparable levels at embryonic day (E)9 and E11 and increased thereafter to reach the highest levels in posthatch chicks. CR-IR neurons were apparent in NM and NA at E11 and in NL by E13, and CR-IR increased in all three auditory nuclei thereafter. Neither unilateral nor bilateral otocyst removal caused detectable changes in the intensity of CR mRNA expression or CR-IR in the auditory nuclei at any of the several ages examined. Similarly, columella removal at posthatching day 2 or 3 failed to significantly affect CR mRNA or CR-IR levels at 3 hours, 1 day, or 3-4 days survival times. We conclude that cochlear nerve input is not necessary for expression of either calretinin mRNA or protein and that the profound decrease in sound-evoked activity caused by columella removal does not affect the maintenance of CR expression after hatching.

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Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei

Cited by 48 publications

References 0 publications

Prevention of Normally Occurring and Deafferentation-Induced Neuronal Death in Chick Brainstem Auditory Neurons by Periodic Blockade of AMPA/Kainate Receptors

Prevention of Normally Occurring and Deafferentation-Induced Neuronal Death in Chick Brainstem Auditory Neurons by Periodic Blockade of AMPA/Kainate Receptors

The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

Calretinin expression in the chick brainstem auditory nuclei develops and is maintained independently of cochlear nerve input

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