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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 odor responses of mitral cells: quantitative analysis.(A) Mean firing rate change evoked by odor stimulation before (control) and during NBQX treatment in the time window between 0.25 and 0.75 s after response onset. Error bars show standard deviation. *, P = 0.02 (sign test). (B) Cumulative distribution of odor-evoked firing rate changes in mitral cells before (control) and during NBQX application. (C) Left: mitral cell odor responses ranked according to the firing rate change measured before NBQX application. Right: Responses of the same mitral cells to the same odors in the presence of NBQX (same rank order as control). Asterisks denote responses that were significantly changed in the presence of NBQX (Student's t-test; P<0.05). (D) Top (continuous lines): average peri-stimulus time histogram of mitral cell odor responses before (control) and during NBQX treatment. Thick portions depict time bins where the peri-stimulus time histogram in the presence of NBQX was significantly different from the control peri-stimulus time histogram in the corresponding time bin (sign test; P<0.05). Dashed lines show standard deviation. (E) Differences of peri-stimulus time histograms (NBQX–control) for all mitral cell odor responses.
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pone-0001416-g004: Effect of NBQX on odor responses of mitral cells: quantitative analysis.(A) Mean firing rate change evoked by odor stimulation before (control) and during NBQX treatment in the time window between 0.25 and 0.75 s after response onset. Error bars show standard deviation. *, P = 0.02 (sign test). (B) Cumulative distribution of odor-evoked firing rate changes in mitral cells before (control) and during NBQX application. (C) Left: mitral cell odor responses ranked according to the firing rate change measured before NBQX application. Right: Responses of the same mitral cells to the same odors in the presence of NBQX (same rank order as control). Asterisks denote responses that were significantly changed in the presence of NBQX (Student's t-test; P<0.05). (D) Top (continuous lines): average peri-stimulus time histogram of mitral cell odor responses before (control) and during NBQX treatment. Thick portions depict time bins where the peri-stimulus time histogram in the presence of NBQX was significantly different from the control peri-stimulus time histogram in the corresponding time bin (sign test; P<0.05). Dashed lines show standard deviation. (E) Differences of peri-stimulus time histograms (NBQX–control) for all mitral cell odor responses.

Mentions: To quantify the effects of NBQX on odor responses we first compared the average odor-evoked firing rate change before and during NBQX treatment between 0.25 s and 0.75 s after response onset. On average, odor stimulation evoked an increase in mitral cell firing of 4.0±9.7 Hz above baseline under control conditions. This increase was significantly enhanced to 11.5±18.9 Hz by NBQX (sign test: P = 0.02; Fig. 4A). The cumulative distribution of response amplitudes was shifted to the right and saturated at higher frequencies (Fig. 4B), showing that smaller responses became less frequent and maximal response magnitudes were increased. However, not all responses were enhanced by NBQX and the effect of NBQX depended on the neuron and stimulus, suggesting that NBQX may also affect the pattern of activity across the population of mitral cells. We therefore compared responses of different mitral cells to different odors before and during application of NBQX in a diagram where responses are ranked according to their magnitude before drug application (Fig. 4C). Response patterns before and during application of NBQX showed obvious similarities, indicating that NBQX did not cause major changes in population activity patterns. Nevertheless, some, but not all, responses in the presence of NBQX were significantly different from control. Thus, the blockade of AMPA/kainate receptors not only scaled odor responses but also caused small changes in the distribution of activity 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 odor responses of mitral cells: quantitative analysis.(A) Mean firing rate change evoked by odor stimulation before (control) and during NBQX treatment in the time window between 0.25 and 0.75 s after response onset. Error bars show standard deviation. *, P = 0.02 (sign test). (B) Cumulative distribution of odor-evoked firing rate changes in mitral cells before (control) and during NBQX application. (C) Left: mitral cell odor responses ranked according to the firing rate change measured before NBQX application. Right: Responses of the same mitral cells to the same odors in the presence of NBQX (same rank order as control). Asterisks denote responses that were significantly changed in the presence of NBQX (Student's t-test; P<0.05). (D) Top (continuous lines): average peri-stimulus time histogram of mitral cell odor responses before (control) and during NBQX treatment. Thick portions depict time bins where the peri-stimulus time histogram in the presence of NBQX was significantly different from the control peri-stimulus time histogram in the corresponding time bin (sign test; P<0.05). Dashed lines show standard deviation. (E) Differences of peri-stimulus time histograms (NBQX–control) for all mitral cell odor responses.
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pone-0001416-g004: Effect of NBQX on odor responses of mitral cells: quantitative analysis.(A) Mean firing rate change evoked by odor stimulation before (control) and during NBQX treatment in the time window between 0.25 and 0.75 s after response onset. Error bars show standard deviation. *, P = 0.02 (sign test). (B) Cumulative distribution of odor-evoked firing rate changes in mitral cells before (control) and during NBQX application. (C) Left: mitral cell odor responses ranked according to the firing rate change measured before NBQX application. Right: Responses of the same mitral cells to the same odors in the presence of NBQX (same rank order as control). Asterisks denote responses that were significantly changed in the presence of NBQX (Student's t-test; P<0.05). (D) Top (continuous lines): average peri-stimulus time histogram of mitral cell odor responses before (control) and during NBQX treatment. Thick portions depict time bins where the peri-stimulus time histogram in the presence of NBQX was significantly different from the control peri-stimulus time histogram in the corresponding time bin (sign test; P<0.05). Dashed lines show standard deviation. (E) Differences of peri-stimulus time histograms (NBQX–control) for all mitral cell odor responses.
Mentions: To quantify the effects of NBQX on odor responses we first compared the average odor-evoked firing rate change before and during NBQX treatment between 0.25 s and 0.75 s after response onset. On average, odor stimulation evoked an increase in mitral cell firing of 4.0±9.7 Hz above baseline under control conditions. This increase was significantly enhanced to 11.5±18.9 Hz by NBQX (sign test: P = 0.02; Fig. 4A). The cumulative distribution of response amplitudes was shifted to the right and saturated at higher frequencies (Fig. 4B), showing that smaller responses became less frequent and maximal response magnitudes were increased. However, not all responses were enhanced by NBQX and the effect of NBQX depended on the neuron and stimulus, suggesting that NBQX may also affect the pattern of activity across the population of mitral cells. We therefore compared responses of different mitral cells to different odors before and during application of NBQX in a diagram where responses are ranked according to their magnitude before drug application (Fig. 4C). Response patterns before and during application of NBQX showed obvious similarities, indicating that NBQX did not cause major changes in population activity patterns. Nevertheless, some, but not all, responses in the presence of NBQX were significantly different from control. Thus, the blockade of AMPA/kainate receptors not only scaled odor responses but also caused small changes in the distribution of activity 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.

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