Glutamatergic and GABAergic agonists increase [Ca2+]i in avian cochlear nucleus neurons

Lachica, E. A.; Kato, Brian; Lippe, William R.; Rubel, Edwin W.

doi:10.1002/(sici)1097-4695(19981105)37:2<321::aid-neu10>3.0.co;2-m

Cited by 16 publications

(24 citation statements)

References 102 publications

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“…In the following years, mGluR-mediated regulation of Ca 2+ signaling in NM neurons was extensively studied, primarily by the same research group (Lachica et al, 1995; 1998; Kato et al, 1996; Zirpel and Rubel 1996; Zirpel et al, 1995, 1998; Kato and Rubel, 1999; Zirpel and Parks, 2001). The key conclusion from these studies is that mGluRs, especially group I mGluRs, play critical roles in regulating Ca 2+ signaling and maintaining Ca 2+ homeostasis and cell survival in NM neurons.…”

Section: Anatomy and Physiology Of Mglurs In Avian Lower Auditory Bramentioning

confidence: 99%

Metabotropic glutamate receptors in auditory processing

2014

Neuroscience

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As the major excitatory neurotransmitter used in the vertebrate brain, glutamate activates ionotropic and metabotropic glutamate receptors (mGluRs), which mediate fast and slow neuronal actions, respectively. Important modulatory roles of mGluRs have been shown in many brain areas, and drugs targeting mGluRs have been developed for treatment of brain disorders. Here, I review the studies on mGluRs in the auditory system. Anatomical expression of mGluRs in the cochlear nucleus has been well characterized, while data for other auditory nuclei await more systematic investigations at both the light and electron microscopy levels. The physiology of mGluRs has been extensively studied using in vitro brain slice preparations, with a focus on the lower auditory brainstem in both mammals and birds. These in vitro physiological studies have revealed that mGluRs participate in neurotransmission, regulate ionic homeostasis, induce synaptic plasticity, and maintain the balance between excitation and inhibition in a variety of auditory structures. However, very few in vivo physiological studies on mGluRs in auditory processing have been undertaken at the systems level. Many questions regarding the essential roles of mGluRs in auditory processing still remain unanswered and more rigorous basic research is warranted.

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Section: Anatomy and Physiology Of Mglurs In Avian Lower Auditory Bramentioning

confidence: 99%

Metabotropic glutamate receptors in auditory processing

2014

Neuroscience

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“…The time course of these AMPA-R EPSCs is attributed to the presence of 'flop' splice variants of the glutamate ionotropic receptor subunits GluR3 and GluR4 and to the relative paucity of subunit GluR2, which together confer faster desensitization kinetics (Dingledine et al, 1999;Geiger et al, 1995;Parks, 2000;Sugden et al, 2002). The absence of GluR2 subunits results in auditory brainstem AMPA receptors that are calcium-permeable (Gardner et al, 1999;Lachica et al, 1998;Otis et al, 1995;Zhou et al, 1995). Immunohistochemical evidence from the barn owl suggests GluR3 and GluR4 are the most prominent AMPA-R subunits in NA (Kubke and Carr, 1998;Levin et al, 1997).…”

Section: Synaptic Mechanisms In Namentioning

confidence: 99%

Beyond timing in the auditory brainstem: intensity coding in the avian cochlear nucleus angularis

MacLeod

Carr

2007

Progress in Brain Research

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IntroductionIndividual acoustic stimulus waveforms in the environment sum together to form a complex composite waveform that arrives at the ear as a single, time-varying pressure amplitude wave. The fundamental problem of hearing lies in how the brain decomposes that waveform into information useful for performing auditory tasks necessary for the survival of the animal such as sound localization and vocal communication. Many of the computational principles for sound localization have emerged from the study of avian brains, especially that of the barn owl, a specialized auditory predator . Additional data from less specialized birds, such as the chicken, and from mammals have revealed a suite of cellular and synaptic specializations in common for the temporal coding of sound, necessary for the detection of one important cue for localization, interaural time difference (ITD): fast glutamatergic neurotransmission, calyceal synaptic morphology, low-threshold voltagegated potassium conductances, bipolar dendritic structures, and axonal delay lines (Carr, 1993;Oertel, 1999;Trussell, 1999). Such commonalities of form arising in widely disparate animal clades suggest that there is a computational advantage to that form, whether it is dendritic structure, expression of a suite of ion channels, or the temporal patterning of activity. Brains in both birds and mammals experience similar constraints in detecting sound, and because hearing of airborne sound arose separately in these two groups, similarities in structure, function and coding between them suggest common coding principles at work, and common solutions arrived at through parallel evolution .A similarly comprehensive answer to the question of coding non-ITD aspects of sound has lagged behind. Early work in the barn owl recognized a division of labor for the coding of interaural timing differences versus interaural intensity differences (also known as interaural level differences, or ILDs), beginning with the two divisions of the avian cochlear nucleus: nucleus magnocellularis (NM) as the origin of the 'timing pathway' and nucleus angularis (NA) as the origin of the 'intensity pathway' ( Figure 1A) (Sullivan and Konishi, 1984;Takahashi et al., 1984); for review see. Both cochlear nuclei are monaural, and project to binaural targets which compare inputs from the two ears (Manley et al., 1988;Takahashi and Konishi, 1988). While NM neurons are similar to the mammalian cochlear nucleus bushy cells, NA is a heterogeneous nucleus with many properties similar to non-bushy cell components of the mammalian cochlear nucleus (CN) Köppl and Carr, 2003;Oertel, 1999;Soares and Carr, 2001;Soares et al., 2002). This heterogeneity (described below) coupled with the extreme specialization of one pathway for timing cues beginning with NM, suggests that NA is largely responsible for encoding non-localization aspects of sound in addition to its role in the ILD pathway. A major challenge will be to * Correspondence should be addressed to: Katrina MacLeod, Department of Biology, Universi...

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“…Although the maximal membrane depolarization induced by activation of the GABAergic system is only approximately 15 mV and the excitatory action can be efficiently prevented by metabotropic glutamate receptor (mGluR)- and GABA B R-mediated modulation (Lu et al, 2005; Lu, 2007), it is conceivable that activation of the GABAergic pathway can cause Ca 2+ entry through low-threshold VGCCs present in NM neurons (Lu and Rubel, 2005). Indeed, application of exogenous GABA does cause [Ca 2+ ] i increases in NM neurons, but the receptors mediating the response remain unclear (Lachica et al, 1998). Finally, activation of mGluRs and GABA B Rs can also contribute to Ca 2+ signaling in NM neurons by stimulating the release of Ca 2+ from intracellular stores and modulating other Ca 2+ pathways (Lachica et al, 1998; Zirpel et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, application of exogenous GABA does cause [Ca 2+ ] i increases in NM neurons, but the receptors mediating the response remain unclear (Lachica et al, 1998). Finally, activation of mGluRs and GABA B Rs can also contribute to Ca 2+ signaling in NM neurons by stimulating the release of Ca 2+ from intracellular stores and modulating other Ca 2+ pathways (Lachica et al, 1998; Zirpel et al, 2000). …”

Section: Introductionmentioning

confidence: 99%

“…To date, studies of intracellular Ca 2+ signaling in NM neurons have focused on the [Ca 2+ ] i increases in response to exogenous agonists for glutamate or GABA receptors (Lachica et al, 1995, 1998; Kato and Rubel, 1999; Zirpel et al, 2000; Diaz et al, 2009). This approach has the advantage of using drugs with known concentrations and known specificity.…”

Section: Introductionmentioning

confidence: 99%

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Synaptic activity-induced Ca2+ signaling in avian cochlear nucleus magnocellularis neurons

Wang

Tang

2012

Neuroscience Research

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Neurons of the avian cochlear nucleus magnocellularis (NM) receive glutamatergic inputs from the spiral ganglion cells via the auditory nerve and feedback GABAergic inputs primarily from the superior olivary nucleus. We investigated regulation of Ca2+ signaling in NM neurons with ratiometric Ca2+ imaging in chicken brain slices. Application of exogenous glutamate or GABA increased the intracellular Ca2+ concentration ([Ca2+]i) in NM neurons. Interestingly, GABA-induced Ca2+ responses persisted into neuronal maturation, in both standard and energy substrate enriched artificial cerebrospinal fluid. More importantly, we found that electrical stimulation applied to the glutamatergic and GABAergic afferent fibers innervating the NM was able to elicit transient [Ca2+]i increases in NM neurons, and the amplitude of the Ca2+ responses increased with increasing frequency and duration of the electrical stimulation. Antagonists for ionotropic glutamate receptors significantly blocked these [Ca2+]i increases, whereas blocking GABAA receptors did not affect the Ca2+ responses, suggesting that synaptically released glutamate but not GABA induced the Ca2+ signaling in vitro. Furthermore, activation of GABAA receptors with exogenous agonists inhibited synaptic activity-induced [Ca2+]i increases in NM neurons, suggesting a role of GABAA receptors in the regulation of Ca2+ homeostasis in the avian cochlear nucleus neurons.

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Glutamatergic and GABAergic agonists increase [Ca2+]i in avian cochlear nucleus neurons

Cited by 16 publications

References 102 publications

Metabotropic glutamate receptors in auditory processing

Metabotropic glutamate receptors in auditory processing

Beyond timing in the auditory brainstem: intensity coding in the avian cochlear nucleus angularis

Synaptic activity-induced Ca2+ signaling in avian cochlear nucleus magnocellularis neurons

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