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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 interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of NBQX (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. ***, P<0.001 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of NBQX. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of NBQX. Data were pooled over all cells, odors and anminals (n = 5878 responses). 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 NBQX. Right: Responses of the same interneurons to the same odors in the presence of NBQX, 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 NBQX treatment is therefore an artifact caused by crowding of bars in the graph.
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pone-0001416-g010: Effect of NBQX on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of NBQX (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. ***, P<0.001 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of NBQX. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of NBQX. Data were pooled over all cells, odors and anminals (n = 5878 responses). 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 NBQX. Right: Responses of the same interneurons to the same odors in the presence of NBQX, 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 NBQX treatment is therefore an artifact caused by crowding of bars in the graph.

Mentions: Somata of interneurons in the deeper layers of the olfactory bulb are densely packed and show pronounced Ca2+ signals in response to odor stimulation (Fig. 10A) [34], [35]. In the presence of NBQX, response amplitudes of many interneurons were decreased and response patterns appeared sparser. Ca2+ signals in the neuropil were also substantially smaller (Fig. 10A). The average somatic Ca2+ signal of interneurons was significantly reduced to 47% of control (sign test: P<0.001; Fig. 10B) and the cumulative distribution of response amplitudes was shifted towards lower amplitudes (Fig. 10C). NBQX therefore increased the ratio between the mean mitral cell response and the mean interneuron response by a factor of 3.2. At the level of individual interneuron somata, the effect of NBQX was diverse. Not all responses were reduced by the same amount, and some responses were even enhanced (Fig. 10A, D, E). The correlation between activity patterns before and during NBQX treatment was 0.41 (n = 5878 responses; pooled over all interneurons and odors) and significantly lower than the correlation between activity patterns in control experiments without drugs (r = 0.71; n = 208 responses; P<0.001). Hence, blockade of AMPA/kainate receptors decreased the mean response of interneurons and changed the activity pattern across the interneuron 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 interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of NBQX (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. ***, P<0.001 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of NBQX. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of NBQX. Data were pooled over all cells, odors and anminals (n = 5878 responses). 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 NBQX. Right: Responses of the same interneurons to the same odors in the presence of NBQX, 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 NBQX 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-g010: Effect of NBQX on interneuron responses measured by 2-photon Ca2+ imaging.(A) Odor-evoked Ca2+ signals in interneurons before, during and after application of NBQX (stimulus: food odor). (B) Average somatic Ca2+ signals before (control) and during application of NBQX, normalized to control. Error bars show standard deviation. ***, P<0.001 (sign test). (C) Cumulative distribution of Ca2+ signal amplitudes before (black) and during (red) application of NBQX. (D) Comparison of Ca2+ signal amplitudes evoked by the same odors in the same interneurons before and during application of NBQX. Data were pooled over all cells, odors and anminals (n = 5878 responses). 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 NBQX. Right: Responses of the same interneurons to the same odors in the presence of NBQX, 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 NBQX treatment is therefore an artifact caused by crowding of bars in the graph.
Mentions: Somata of interneurons in the deeper layers of the olfactory bulb are densely packed and show pronounced Ca2+ signals in response to odor stimulation (Fig. 10A) [34], [35]. In the presence of NBQX, response amplitudes of many interneurons were decreased and response patterns appeared sparser. Ca2+ signals in the neuropil were also substantially smaller (Fig. 10A). The average somatic Ca2+ signal of interneurons was significantly reduced to 47% of control (sign test: P<0.001; Fig. 10B) and the cumulative distribution of response amplitudes was shifted towards lower amplitudes (Fig. 10C). NBQX therefore increased the ratio between the mean mitral cell response and the mean interneuron response by a factor of 3.2. At the level of individual interneuron somata, the effect of NBQX was diverse. Not all responses were reduced by the same amount, and some responses were even enhanced (Fig. 10A, D, E). The correlation between activity patterns before and during NBQX treatment was 0.41 (n = 5878 responses; pooled over all interneurons and odors) and significantly lower than the correlation between activity patterns in control experiments without drugs (r = 0.71; n = 208 responses; P<0.001). Hence, blockade of AMPA/kainate receptors decreased the mean response of interneurons and changed the activity pattern across the interneuron 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