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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 NBQX on mitral cell responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in mitral cells before, during and after application of NBQX (stimulus: Trp, 10 µM). Arrows depict somata of neurons identified as mitral cells by expression of the genetically encoded fluorescence marker HuC-YC. (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. **, P = 0.002 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during application of NBQX (red) and after washout (gray). (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same mitral cells before and during application of NBQX. Data were pooled over all cells, odors and animals (n = 190 responses). r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: mitral cell odor responses ranked according to the Ca2+ signal before application of NBQX. Inset shows an enlargement of a subregion. Right: Responses of the same mitral cells to the same odors in the presence of NBQX, ranked in the same order as in the control.
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pone-0001416-g008: Effect of NBQX on mitral cell responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in mitral cells before, during and after application of NBQX (stimulus: Trp, 10 µM). Arrows depict somata of neurons identified as mitral cells by expression of the genetically encoded fluorescence marker HuC-YC. (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. **, P = 0.002 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during application of NBQX (red) and after washout (gray). (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same mitral cells before and during application of NBQX. Data were pooled over all cells, odors and animals (n = 190 responses). r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: mitral cell odor responses ranked according to the Ca2+ signal before application of NBQX. Inset shows an enlargement of a subregion. Right: Responses of the same mitral cells to the same odors in the presence of NBQX, ranked in the same order as in the control.

Mentions: We first examined the effect of glutamate receptor antagonists on odor-evoked Ca2+ signals of mitral cells using the same drug application protocol as before (Fig. 8A). In many mitral cells, NBQX increased the amplitude of odor-evoked Ca2+ signals, while decreases in response amplitude were rarely observed. On average, NBQX significantly increased Ca2+ signals to 150% of control (sign test: P = 0.002; Fig. 8B). Consequently, the cumulative distribution of response amplitudes was shifted towards higher amplitudes (Fig. 8C). At the level of individual mitral cells, the effect of NBQX varied in magnitude (Fig. 8D, E). The correlation between mitral cell activity patterns before and during NBQX treatment was 0.73 (Fig. 8D; n = 190 responses; pooled over all mitral cells and odors). As a control, we performed the same procedures in a different set of fish except that NBQX was omitted during the wash-in period. The correlation between activity patterns in these control experiments (r = 0.78; n = 126 responses) was slightly, but not significantly (P = 0.32), higher than in experiments using NBQX. Hence, NBQX increased the amplitude of the mitral cell population response but had little or no effect on the odor-evoked pattern of Ca2+ signals across the mitral cell population.


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

Tabor R, Friedrich RW - PLoS ONE (2008)

Effect of NBQX on mitral cell responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in mitral cells before, during and after application of NBQX (stimulus: Trp, 10 µM). Arrows depict somata of neurons identified as mitral cells by expression of the genetically encoded fluorescence marker HuC-YC. (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. **, P = 0.002 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during application of NBQX (red) and after washout (gray). (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same mitral cells before and during application of NBQX. Data were pooled over all cells, odors and animals (n = 190 responses). r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: mitral cell odor responses ranked according to the Ca2+ signal before application of NBQX. Inset shows an enlargement of a subregion. Right: Responses of the same mitral cells to the same odors in the presence of NBQX, ranked in the same order as in the control.
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pone-0001416-g008: Effect of NBQX on mitral cell responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in mitral cells before, during and after application of NBQX (stimulus: Trp, 10 µM). Arrows depict somata of neurons identified as mitral cells by expression of the genetically encoded fluorescence marker HuC-YC. (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. **, P = 0.002 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during application of NBQX (red) and after washout (gray). (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same mitral cells before and during application of NBQX. Data were pooled over all cells, odors and animals (n = 190 responses). r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: mitral cell odor responses ranked according to the Ca2+ signal before application of NBQX. Inset shows an enlargement of a subregion. Right: Responses of the same mitral cells to the same odors in the presence of NBQX, ranked in the same order as in the control.
Mentions: We first examined the effect of glutamate receptor antagonists on odor-evoked Ca2+ signals of mitral cells using the same drug application protocol as before (Fig. 8A). In many mitral cells, NBQX increased the amplitude of odor-evoked Ca2+ signals, while decreases in response amplitude were rarely observed. On average, NBQX significantly increased Ca2+ signals to 150% of control (sign test: P = 0.002; Fig. 8B). Consequently, the cumulative distribution of response amplitudes was shifted towards higher amplitudes (Fig. 8C). At the level of individual mitral cells, the effect of NBQX varied in magnitude (Fig. 8D, E). The correlation between mitral cell activity patterns before and during NBQX treatment was 0.73 (Fig. 8D; n = 190 responses; pooled over all mitral cells and odors). As a control, we performed the same procedures in a different set of fish except that NBQX was omitted during the wash-in period. The correlation between activity patterns in these control experiments (r = 0.78; n = 126 responses) was slightly, but not significantly (P = 0.32), higher than in experiments using NBQX. Hence, NBQX increased the amplitude of the mitral cell population response but had little or no effect on the odor-evoked pattern of Ca2+ signals across the mitral cell population.

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.

Show MeSH
Related in: MedlinePlus