Glutamate receptor subunits in neuronal populations of the gerbil lateral superior olive

Schwartz, Ilsa R.; Eager, Patricia R.

doi:10.1016/s0378-5955(99)00140-9

Cited by 14 publications

(8 citation statements)

References 48 publications

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“…The expression levels were evaluated semiquantitatively on the single-cell level which allows for an estimation of the relative amounts of AMPA receptor subunits expressed in neuronal populations of auditory nuclei. The distribution of subunits in the auditory brainstem and midbrain, as observed in the present study, is in general agreement with previous immunocytochemical (Petralia et al, 1996;Gaza and Ribak, 1997;Levin et al, 1997;Caicedo and Eybalin, 1999;Schwartz and Eager, 1999) and in situ hybridization studies (Hunter et al, 1993;Wang et al, 1998) of both mammals and birds. However, these studies failed to differentiate between the flip/flop splice variants and the GluR-B and -C subunits.…”

Section: Class II Includes Nuclei That Show a Predominant Expression supporting

confidence: 93%

“…However, our present data demonstrate only low levels of the GluR-B subunit in MNTB neurons. Low GluR-B subunit expression was also shown by Caicedo and Eybalin (1999), Schwartz and Eager (1999), and Wang et al (1998), who employed specific antibodies against GluR-B/C and GluR-B only. The fact that MNTB neurons have a high calcium permeability (Geiger et al, 1995) and take up Ca 2ϩ ions through AMPA receptors (Zhou et al, 1995;Caicedo et al, 1998) further indicates that MNTB neurons express predominantly AMPA receptors lacking the GluR-B subunit (Hollmann et al, 1991;Lomeli et al, 1994;Petralia et al, 1997;Washburn et al, 1997).…”

Section: Class II Includes Nuclei That Show a Predominant Expression mentioning

confidence: 73%

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Expression of AMPA receptor subunit flip/flop splice variants in the rat auditory brainstem and inferior colliculus

Schmid¹,

Guthmann²,

Ruppersberg³

et al. 2001

J. Comp. Neurol.

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The expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor subunit mRNAs and their flip/flop splice variants was evaluated in the rat auditory brainstem and inferior colliculus employing in situ hybridization with radiolabeled oligonucleotide probes. A differential expression of AMPA receptor subunits in auditory nuclei was observed. In general, neurons in all nuclei of the auditory brainstem express high levels of GluR-C flop and GluR-D flop mRNA, but low to very low levels of GluR-A and GluR-B mRNA. The strongest GluR-C and -D flop expression is found in the ventral and medial part of the anteroventral cochlear nucleus, the posteroventral cochlear nucleus, and the medial and the lateral superior olive. These nuclei are part of the binaural auditory pathway which is important for sound localization in space. In contrast, neurons in the central nucleus of the inferior colliculus express high levels of GluR-B flip but only low levels of the other AMPA receptor subunits. From our data, we conclude that neurons of nuclei involved in binaural processing exhibit a specific "auditory AMPA receptor" which consists primarily of GluR-C flop and -D flop and often lacks GluR-B subunits; this indicates fast kinetics and high Ca(2+) permeability of AMPA receptor currents. In contrast, neurons in the central nucleus of the inferior colliculus contain large amounts of GluR-B flip subunits resulting in Ca(2+) impermeable AMPA receptors with slow kinetics.

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Section: Class II Includes Nuclei That Show a Predominant Expression supporting

confidence: 93%

Section: Class II Includes Nuclei That Show a Predominant Expression mentioning

confidence: 73%

Expression of AMPA receptor subunit flip/flop splice variants in the rat auditory brainstem and inferior colliculus

Schmid¹,

Guthmann²,

Ruppersberg³

et al. 2001

J. Comp. Neurol.

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“…Group II mGluRs (mGluR2 and mGluR3) and group III mGluRs (mGluR4 and mGluR6 -8) are associated with G i/o -type proteins and generally are negatively coupled to adenylate cyclase activity. In the auditory brain stem, group I and II mGluRs are expressed in several auditory nuclei (Bilak and Morest 1998;Elezgarai et al 1999Elezgarai et al , 2001Jaarsma et al 1998;Molitor and Manis 1997;Schwartz and Eager 1999;Takahashi et al 1996;Zirpel et al 2000;reviewed in Petralia et al 2000). In the LSO, electrophysiological recordings have indicated expression of group II and/or III mGluRs on presynaptic glutamatergic terminals (Wu and Fu 1998) and group I mGluRs on postsynaptic LSO neurons (Kotak and Sanes 1995).…”

Section: Metabotropic Glutamate Receptor-mediated Ca 2ϩ Responsesmentioning

confidence: 99%

“…A number of studies in other neuronal systems have demonstrated the central role of calcium-dependent mechanisms in mediating the effects of activity on neuronal survival and development (Berridge 1998;Franklin and Johnson 1992;Spitzer et al 2000). In the developing auditory system, the role of calcium-dependent mechanisms in activity-dependent neuronal survival is best understood in the cochlear nucleus of chickens.…”

Section: Introductionmentioning

confidence: 99%

Glutamatergic Calcium Responses in the Developing Lateral Superior Olive: Receptor Types and Their Specific Activation by Synaptic Activity Patterns

Ene

Kullmann

Gillespie

et al. 2003

Journal of Neurophysiology

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calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns. J Neurophysiol 90: 2581-2591, 2003. First published July 9, 2003 10.1152/jn.00238.2003. The lateral superior olive (LSO) is a binaural auditory brain stem nucleus that plays a central role in sound localization. Survival and maturation of developing LSO neurons critically depend on intracellular calcium signaling. Here we investigated the mechanisms by which glutamatergic afferents from the cochlear nucleus increase intracellular calcium concentration in LSO neurons. Using fura-2 calcium imaging in slices prepared from neonatal mice, we found that cochlear nucleus afferents can activate all major classes of ionotropic and metabotropic glutamate receptors, each of which contributes to an increase in intracellular calcium. The specific activation of different glutamate receptor classes was dependent on response amplitudes and afferent stimulus patterns. Lowamplitude responses elicited by single stimuli were entirely mediated by calcium-impermeable AMPA/kainate receptors that activated voltage-gated calcium channels. Larger-amplitude responses elicited by either single stimuli or stimulus trains resulted in additional calcium influx through N-methyl-D-aspartate receptors. Finally, high-frequency stimulation also recruited group I and group II metabotropic glutamate receptors, both of which mobilized intracellular calcium. This calcium release in turn activated a strong influx of extracellular calcium through a membrane calcium channel that is distinct from voltage-gated calcium channels. Together, these results indicate that before hearing onset, distinct patterns of afferent activity generate qualitatively distinct types of calcium responses, which likely serve in guiding different aspects of LSO development. I N T R O D U C T I O NOne of the major functions of the auditory system is to determine the direction of incoming sound. The lateral superior olive (LSO) is the first station in the ascending auditory pathway that processes interaural intensity differences (Boudreau and Tsuchitani 1970;Caird and Klinke 1983; for review, see Oertel 1999). Neurons in this nucleus are excited by sound at the ipsilateral ear and are inhibited by sound at the contralateral ear. Excitation reaches the LSO via a glutamatergic projection from spherical bushy cells in the ipsilateral anteroventral cochlear nucleus (AVCN, reviewed in Thompson and Schofield 2000). Inhibition reaches the LSO via a glycinergic projection from the medial nucleus of the trapezoid body (MNTB). Both excitatory and inhibitory inputs are tonotopically organized and converge on single LSO neurons in a precise frequencyspecific manner (Oertel 1999;Sanes and Rubel 1988).Normal development of the LSO depends on the presence of afferent inputs and synaptic activity (reviewed in Sanes and Friauf 2000). Abolishing the ipsilateral excitatory inputs by cochlea ablation decreases LSO volume and cell number (Moore 1992) and reduces exc...

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“…To emulate synaptic currents from proximal and distal dendrites, we used a current‐clamp protocol consisting of stimulation of synaptic terminals concomitantly with current injection via somatic patch pipettes. The latter would simulate synaptic currents arising from the proximal dendrite (Ulrich & Stricker, 2000) as excitatory pre‐synaptic terminals were found all along LSO principal cell dendrites (Schwartz & Eager, 1999). Confined to peri‐somatic compartments (dynamic clamp), I h caused an increase in cell excitability when compared with conditions in which native I h was intact.…”

Section: Discussionmentioning

confidence: 99%

Modulation of dendritic synaptic processing in the lateral superior olive by hyperpolarization-activated currents

Leão

Walmsley

2011

European Journal of Neuroscience

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We have previously shown that mice lateral superior olive (LSO) neurons exhibit a large hyperpolarization-activated current (I h ), and that hyperpolarization-activated cyclic-nucleotide-gated type 1 channels are present in both the soma and dendrites of these cells. Here we show that the dendritic I h in LSO neurons modulates the integration of multiple synaptic inputs. We tested the LSO neuron's ability to integrate synaptic inputs by evoking excitatory post-synaptic potentials (EPSPs) in conjunction with brief depolarizing current pulses (to simulate a second excitatory input) at different time delays. We compared LSO neurons with the native I h present in both the soma and dendrites (control) with LSO neurons without I h (blocked with ZD7288) and with LSO neurons with I h only present perisomatically (ZD7288+ computer-simulated I h using a dynamic clamp). LSO neurons without I h had a wider time window for firing in response to inputs with short time separations. Simulated somatic I h (dynamic clamp) could not reverse this effect. Blocking I h also increased the summation of EPSPs elicited at both proximal and distal dendritic regions, and dramatically altered the integration of EPSPs and inhibitory post-synaptic potentials. The addition of simulated peri-somatic I h could not abolish a ZD7288-induced increase of responsiveness to widely separated excitatory inputs. Using a compartmental LSO model, we show that dendritic I h can reduce EPSP integration by locally decreasing the input resistance. Our results suggest a significant role for dendritic I h in LSO neurons, where the activation ⁄ deactivation of I h can alter the LSO response to synaptic inputs.

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Glutamate receptor subunits in neuronal populations of the gerbil lateral superior olive

Cited by 14 publications

References 48 publications

Expression of AMPA receptor subunit flip/flop splice variants in the rat auditory brainstem and inferior colliculus

Expression of AMPA receptor subunit flip/flop splice variants in the rat auditory brainstem and inferior colliculus

Glutamatergic Calcium Responses in the Developing Lateral Superior Olive: Receptor Types and Their Specific Activation by Synaptic Activity Patterns

Modulation of dendritic synaptic processing in the lateral superior olive by hyperpolarization-activated currents

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