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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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Effect of the AMPA/kainate receptor antagonist, NBQX, on odor responses of mitral cells.(A) Whole-cell recording of a mitral cell response to odor stimulation (food extract; bar) before (black) and during (red) bath-application of NBQX and after washout (gray). (B1–B5) Five examples illustrating effects of NBQX on odor responses. Ticks denote individual action potentials. Each row shows one trial. Black: control; red: during NBQX application; gray: after wash-out of NBQX. Continuous lines are peri-stimulus time histograms, averaged over all trials under each condition. Thick portions depict time bins where peri-stimulus time histograms were significantly different (Student's t-test; P<0.05) from the corresponding time bin in the control peri-stimulus time histogram (black). Bar indicates odor stimulation. Responses are from different cells and were recorded in the whole-cell, cell-attached or loose-patch configuration.
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pone-0001416-g003: Effect of the AMPA/kainate receptor antagonist, NBQX, on odor responses of mitral cells.(A) Whole-cell recording of a mitral cell response to odor stimulation (food extract; bar) before (black) and during (red) bath-application of NBQX and after washout (gray). (B1–B5) Five examples illustrating effects of NBQX on odor responses. Ticks denote individual action potentials. Each row shows one trial. Black: control; red: during NBQX application; gray: after wash-out of NBQX. Continuous lines are peri-stimulus time histograms, averaged over all trials under each condition. Thick portions depict time bins where peri-stimulus time histograms were significantly different (Student's t-test; P<0.05) from the corresponding time bin in the control peri-stimulus time histogram (black). Bar indicates odor stimulation. Responses are from different cells and were recorded in the whole-cell, cell-attached or loose-patch configuration.

Mentions: In contrast to the combined application of AMPA/kainate and NMDA receptor antagonists, the selective blockade of AMPA/kainate receptors by NBQX produced diverse effects on mitral cell activity. The spontaneous activity of individual mitral cells could decrease, remain similar, or even increase relative to control levels. On average, NBQX did not significantly change the spontaneous firing rate. Average spontaneous firing rates under control conditions and in the presence of NBQX were 6.6±3.61 Hz (mean±standard deviation) and 5.51±4.90 Hz, respectively (sign test: p = 0.23; n = 13 mitral cells). In most (5/6) mitral cells, steep subthreshold transients in the membrane potential were strongly reduced while slow fluctuations could still be observed (Fig. 3A).


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

Tabor R, Friedrich RW - PLoS ONE (2008)

Effect of the AMPA/kainate receptor antagonist, NBQX, on odor responses of mitral cells.(A) Whole-cell recording of a mitral cell response to odor stimulation (food extract; bar) before (black) and during (red) bath-application of NBQX and after washout (gray). (B1–B5) Five examples illustrating effects of NBQX on odor responses. Ticks denote individual action potentials. Each row shows one trial. Black: control; red: during NBQX application; gray: after wash-out of NBQX. Continuous lines are peri-stimulus time histograms, averaged over all trials under each condition. Thick portions depict time bins where peri-stimulus time histograms were significantly different (Student's t-test; P<0.05) from the corresponding time bin in the control peri-stimulus time histogram (black). Bar indicates odor stimulation. Responses are from different cells and were recorded in the whole-cell, cell-attached or loose-patch configuration.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169298&req=5

pone-0001416-g003: Effect of the AMPA/kainate receptor antagonist, NBQX, on odor responses of mitral cells.(A) Whole-cell recording of a mitral cell response to odor stimulation (food extract; bar) before (black) and during (red) bath-application of NBQX and after washout (gray). (B1–B5) Five examples illustrating effects of NBQX on odor responses. Ticks denote individual action potentials. Each row shows one trial. Black: control; red: during NBQX application; gray: after wash-out of NBQX. Continuous lines are peri-stimulus time histograms, averaged over all trials under each condition. Thick portions depict time bins where peri-stimulus time histograms were significantly different (Student's t-test; P<0.05) from the corresponding time bin in the control peri-stimulus time histogram (black). Bar indicates odor stimulation. Responses are from different cells and were recorded in the whole-cell, cell-attached or loose-patch configuration.
Mentions: In contrast to the combined application of AMPA/kainate and NMDA receptor antagonists, the selective blockade of AMPA/kainate receptors by NBQX produced diverse effects on mitral cell activity. The spontaneous activity of individual mitral cells could decrease, remain similar, or even increase relative to control levels. On average, NBQX did not significantly change the spontaneous firing rate. Average spontaneous firing rates under control conditions and in the presence of NBQX were 6.6±3.61 Hz (mean±standard deviation) and 5.51±4.90 Hz, respectively (sign test: p = 0.23; n = 13 mitral cells). In most (5/6) mitral cells, steep subthreshold transients in the membrane potential were strongly reduced while slow fluctuations could still be observed (Fig. 3A).

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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