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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 AP5 on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of AP5 (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of AP5, normalized to control. Error bars show standard deviation. (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of AP5. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of AP5. r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: interneuron odor responses ranked according to the Ca2+ signal before application of AP5. Data were pooled over all cells, odors and anminals (n = 14884 responses). Right: Responses of the same interneurons to the same odors in the presence of AP5, ranked in the same order as in the control. Inset shows an enlargement of a subregion to demonstrate that low-amplitude values are interspersed between high amplitude values. The visual impression in the full diagram that many amplitudes are increased during AP5 treatment is therefore an artifact caused by crowding of bars in the graph.
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pone-0001416-g011: Effect of AP5 on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of AP5 (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of AP5, normalized to control. Error bars show standard deviation. (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of AP5. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of AP5. r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: interneuron odor responses ranked according to the Ca2+ signal before application of AP5. Data were pooled over all cells, odors and anminals (n = 14884 responses). Right: Responses of the same interneurons to the same odors in the presence of AP5, ranked in the same order as in the control. Inset shows an enlargement of a subregion to demonstrate that low-amplitude values are interspersed between high amplitude values. The visual impression in the full diagram that many amplitudes are increased during AP5 treatment is therefore an artifact caused by crowding of bars in the graph.

Mentions: Blockade of NMDA receptors by AP5 caused only a slight change in the mean response amplitude of interneurons to 109% of control (sign test: P<0.001; Fig. 11A, B) and the cumulative histogram of response amplitudes remained similar (Fig. 11C). AP5 therefore changed the ratio between the mean mitral cell response and the mean interneuron response by a factor of 0.79. Individual interneuron responses, however, were often increased or decreased by AP5 (Fig. 11D, E). The correlation between activity patterns before and during AP5 treatment was 0.40 (n = 14884 responses) and significantly different from control (r = 0.71; n = 208 responses; P<0.001). Hence, the blockade of NMDA receptors had little effect on the overall amplitude of interneuron responses but caused a redistribution of activity across the 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 AP5 on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of AP5 (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of AP5, normalized to control. Error bars show standard deviation. (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of AP5. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of AP5. r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: interneuron odor responses ranked according to the Ca2+ signal before application of AP5. Data were pooled over all cells, odors and anminals (n = 14884 responses). Right: Responses of the same interneurons to the same odors in the presence of AP5, ranked in the same order as in the control. Inset shows an enlargement of a subregion to demonstrate that low-amplitude values are interspersed between high amplitude values. The visual impression in the full diagram that many amplitudes are increased during AP5 treatment is therefore an artifact caused by crowding of bars in the graph.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169298&req=5

pone-0001416-g011: Effect of AP5 on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of AP5 (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of AP5, normalized to control. Error bars show standard deviation. (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of AP5. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of AP5. r, Pearson correlation coefficient. Inset shows the density of data points in the boxed region. Lines are diagonals with slope one. (E) Left: interneuron odor responses ranked according to the Ca2+ signal before application of AP5. Data were pooled over all cells, odors and anminals (n = 14884 responses). Right: Responses of the same interneurons to the same odors in the presence of AP5, ranked in the same order as in the control. Inset shows an enlargement of a subregion to demonstrate that low-amplitude values are interspersed between high amplitude values. The visual impression in the full diagram that many amplitudes are increased during AP5 treatment is therefore an artifact caused by crowding of bars in the graph.
Mentions: Blockade of NMDA receptors by AP5 caused only a slight change in the mean response amplitude of interneurons to 109% of control (sign test: P<0.001; Fig. 11A, B) and the cumulative histogram of response amplitudes remained similar (Fig. 11C). AP5 therefore changed the ratio between the mean mitral cell response and the mean interneuron response by a factor of 0.79. Individual interneuron responses, however, were often increased or decreased by AP5 (Fig. 11D, E). The correlation between activity patterns before and during AP5 treatment was 0.40 (n = 14884 responses) and significantly different from control (r = 0.71; n = 208 responses; P<0.001). Hence, the blockade of NMDA receptors had little effect on the overall amplitude of interneuron responses but caused a redistribution of activity across the 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