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Pharmacological analysis of ionotropic glutamate receptor function in neuronal circuits of the zebrafish olfactory bulb.

Tabor R, Friedrich RW - PLoS ONE (2008)

Bottom Line: However, antagonists of both receptor types had diverse effects on the magnitude and time course of individual mitral cell and interneuron responses and, thus, changed spatio-temporal activity patterns across neuronal populations.Oscillatory synchronization was abolished or reduced by AMPA/kainate and NMDA receptor antagonists, respectively.These results indicate that (1) interneuron responses depend mainly on AMPA/kainate receptor input during an odor response, (2) interactions among mitral cells and interneurons regulate the total olfactory bulb output activity, (3) AMPA/kainate receptors participate in the synchronization of odor-dependent neuronal ensembles, and (4) ionotropic glutamate receptor-containing synaptic circuits shape odor-specific patterns of olfactory bulb output activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Optics, Max-Planck-Institute for Medical Research, Heidelberg, Germany.

ABSTRACT
Although synaptic functions of ionotropic glutamate receptors in the olfactory bulb have been studied in vitro, their roles in pattern processing in the intact system remain controversial. We therefore examined the functions of ionotropic glutamate receptors during odor processing in the intact olfactory bulb of zebrafish using pharmacological manipulations. Odor responses of mitral cells and interneurons were recorded by electrophysiology and 2-photon Ca(2+) imaging. The combined blockade of AMPA/kainate and NMDA receptors abolished odor-evoked excitation of mitral cells. The blockade of AMPA/kainate receptors alone, in contrast, increased the mean response of mitral cells and decreased the mean response of interneurons. The blockade of NMDA receptors caused little or no change in the mean responses of mitral cells and interneurons. However, antagonists of both receptor types had diverse effects on the magnitude and time course of individual mitral cell and interneuron responses and, thus, changed spatio-temporal activity patterns across neuronal populations. Oscillatory synchronization was abolished or reduced by AMPA/kainate and NMDA receptor antagonists, respectively. These results indicate that (1) interneuron responses depend mainly on AMPA/kainate receptor input during an odor response, (2) interactions among mitral cells and interneurons regulate the total olfactory bulb output activity, (3) AMPA/kainate receptors participate in the synchronization of odor-dependent neuronal ensembles, and (4) ionotropic glutamate receptor-containing synaptic circuits shape odor-specific patterns of olfactory bulb output activity. These mechanisms are likely to be important for the processing of odor-encoding activity patterns in the olfactory bulb.

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Ionotropic glutamate receptors are essential for odor responses of mitral cells.(A) Whole-cell recording from a mitral cell during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5. (B) Local field potential recording during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5 and after washout (gray). Traces are band-pass filtered between 8–43 Hz. (C) Power spectrum of local field potential traces (average of 6 trials; from unfiltered data) for the examples shown in (B). (D) Average local field potential power (15–30 Hz) in the presence of NBQX and AP5, normalized to control (n = 4 olfactory bulbs). ***, P<0.001.
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pone-0001416-g002: Ionotropic glutamate receptors are essential for odor responses of mitral cells.(A) Whole-cell recording from a mitral cell during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5. (B) Local field potential recording during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5 and after washout (gray). Traces are band-pass filtered between 8–43 Hz. (C) Power spectrum of local field potential traces (average of 6 trials; from unfiltered data) for the examples shown in (B). (D) Average local field potential power (15–30 Hz) in the presence of NBQX and AP5, normalized to control (n = 4 olfactory bulbs). ***, P<0.001.

Mentions: In the presence of NBQX and AP5, spontaneous action potential firing was either completely abolished or became slow and periodic (n = 4 mitral cells; Fig. 2A). Subthreshold membrane potential fluctuations were reduced or eliminated and spontaneous fluctuations in the local field potential were decreased (Fig. 2A, B). Odor stimulation failed to elicit mitral cell depolarization and action potential firing (Fig. 2A). Similar results were obtained in all mitral cells, each of which was stimulated with 1–2 amino acid odors or food extracts that elicited a strong response under control conditions. Moreover, odor-evoked local field potential oscillations were completely abolished (Fig. 2B, C, D). In the presence of NBQX and AP5, the power in the 15–30 Hz band of the local field potential was significantly reduced to 4±1% of control (t-test: P<0.001). These results show that glutamatergic synaptic transmission is essential for responses of olfactory bulb neurons to odors, most likely because glutamate is the neurotransmitter of olfactory sensory neurons [30], [31].


Pharmacological analysis of ionotropic glutamate receptor function in neuronal circuits of the zebrafish olfactory bulb.

Tabor R, Friedrich RW - PLoS ONE (2008)

Ionotropic glutamate receptors are essential for odor responses of mitral cells.(A) Whole-cell recording from a mitral cell during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5. (B) Local field potential recording during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5 and after washout (gray). Traces are band-pass filtered between 8–43 Hz. (C) Power spectrum of local field potential traces (average of 6 trials; from unfiltered data) for the examples shown in (B). (D) Average local field potential power (15–30 Hz) in the presence of NBQX and AP5, normalized to control (n = 4 olfactory bulbs). ***, P<0.001.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169298&req=5

pone-0001416-g002: Ionotropic glutamate receptors are essential for odor responses of mitral cells.(A) Whole-cell recording from a mitral cell during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5. (B) Local field potential recording during odor stimulation (food extract; bar) before (black) and during (red) application of NBQX and AP5 and after washout (gray). Traces are band-pass filtered between 8–43 Hz. (C) Power spectrum of local field potential traces (average of 6 trials; from unfiltered data) for the examples shown in (B). (D) Average local field potential power (15–30 Hz) in the presence of NBQX and AP5, normalized to control (n = 4 olfactory bulbs). ***, P<0.001.
Mentions: In the presence of NBQX and AP5, spontaneous action potential firing was either completely abolished or became slow and periodic (n = 4 mitral cells; Fig. 2A). Subthreshold membrane potential fluctuations were reduced or eliminated and spontaneous fluctuations in the local field potential were decreased (Fig. 2A, B). Odor stimulation failed to elicit mitral cell depolarization and action potential firing (Fig. 2A). Similar results were obtained in all mitral cells, each of which was stimulated with 1–2 amino acid odors or food extracts that elicited a strong response under control conditions. Moreover, odor-evoked local field potential oscillations were completely abolished (Fig. 2B, C, D). In the presence of NBQX and AP5, the power in the 15–30 Hz band of the local field potential was significantly reduced to 4±1% of control (t-test: P<0.001). These results show that glutamatergic synaptic transmission is essential for responses of olfactory bulb neurons to odors, most likely because glutamate is the neurotransmitter of olfactory sensory neurons [30], [31].

Bottom Line: However, antagonists of both receptor types had diverse effects on the magnitude and time course of individual mitral cell and interneuron responses and, thus, changed spatio-temporal activity patterns across neuronal populations.Oscillatory synchronization was abolished or reduced by AMPA/kainate and NMDA receptor antagonists, respectively.These results indicate that (1) interneuron responses depend mainly on AMPA/kainate receptor input during an odor response, (2) interactions among mitral cells and interneurons regulate the total olfactory bulb output activity, (3) AMPA/kainate receptors participate in the synchronization of odor-dependent neuronal ensembles, and (4) ionotropic glutamate receptor-containing synaptic circuits shape odor-specific patterns of olfactory bulb output activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Optics, Max-Planck-Institute for Medical Research, Heidelberg, Germany.

ABSTRACT
Although synaptic functions of ionotropic glutamate receptors in the olfactory bulb have been studied in vitro, their roles in pattern processing in the intact system remain controversial. We therefore examined the functions of ionotropic glutamate receptors during odor processing in the intact olfactory bulb of zebrafish using pharmacological manipulations. Odor responses of mitral cells and interneurons were recorded by electrophysiology and 2-photon Ca(2+) imaging. The combined blockade of AMPA/kainate and NMDA receptors abolished odor-evoked excitation of mitral cells. The blockade of AMPA/kainate receptors alone, in contrast, increased the mean response of mitral cells and decreased the mean response of interneurons. The blockade of NMDA receptors caused little or no change in the mean responses of mitral cells and interneurons. However, antagonists of both receptor types had diverse effects on the magnitude and time course of individual mitral cell and interneuron responses and, thus, changed spatio-temporal activity patterns across neuronal populations. Oscillatory synchronization was abolished or reduced by AMPA/kainate and NMDA receptor antagonists, respectively. These results indicate that (1) interneuron responses depend mainly on AMPA/kainate receptor input during an odor response, (2) interactions among mitral cells and interneurons regulate the total olfactory bulb output activity, (3) AMPA/kainate receptors participate in the synchronization of odor-dependent neuronal ensembles, and (4) ionotropic glutamate receptor-containing synaptic circuits shape odor-specific patterns of olfactory bulb output activity. These mechanisms are likely to be important for the processing of odor-encoding activity patterns in the olfactory bulb.

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