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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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Simplified architecture of synaptic pathways in the olfactory bulb.Within glomeruli, glutamatergic olfactory sensory neurons provide excitatory synaptic input to mitral cells and a subpopulation of periglomerular cells via AMPA/kainate and NMDA receptors. Periglomerular cells also receive glutamatergic input from mitral cell dendrites and provide GABAergic output to mitral cells of the same and neighbouring glomeruli. In addition, GABA (green arrow) and dopamine (not shown) released from periglomerular cells reduces glutamate release from olfactory sensory neuron axon terminals by acting on GABAB and D2 receptors, respectively, in the same glomerulus [23], [49]–[53]. In subglomerular layers, glutamate release from mitral cell dendrites and axon collaterals stimulates granule cells via AMPA/kainate and NMDA receptors. Granule cells release GABA back onto GABAA receptors on the same and other mitral cells. Glutamate release from a mitral cell can therefore cause recurrent inhibition of the same mitral cell and lateral inhibition of other mitral cells via periglomerular and granule cells. These interactions, here collectively referred to as the mitral cell→interneuron→mitral cell pathway, can extend over distances corresponding to multiple glomeruli. An additional pathway mediating lateral inhibition that is not detailed in this scheme is the short axon cell (SAC)→periglomerular→mitral cell pathway identified in rodents [13], [54]. Centrifugal inputs from higher brain areas are also not shown in detail. Many of these inputs terminate on interneurons and are glutamatergic. Not included in the scheme are metabotropic glutamate receptors, interactions among interneurons in the granule cell layer [55], glutamate spillover [56], and a small glutamatergic subpopulation of granule cells [57]. Strong excitatory interactions across glomeruli, as revealed in the antennal lobe of Drosophila [58]–[60], have not been found in the vertebrate olfactory bulb. Abbreviations: OSN: olfactory sensory neuron, PGC: periglomerular cell, MC: mitral cell, GC: granule cell, SAC: short axon cell.
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pone-0001416-g001: Simplified architecture of synaptic pathways in the olfactory bulb.Within glomeruli, glutamatergic olfactory sensory neurons provide excitatory synaptic input to mitral cells and a subpopulation of periglomerular cells via AMPA/kainate and NMDA receptors. Periglomerular cells also receive glutamatergic input from mitral cell dendrites and provide GABAergic output to mitral cells of the same and neighbouring glomeruli. In addition, GABA (green arrow) and dopamine (not shown) released from periglomerular cells reduces glutamate release from olfactory sensory neuron axon terminals by acting on GABAB and D2 receptors, respectively, in the same glomerulus [23], [49]–[53]. In subglomerular layers, glutamate release from mitral cell dendrites and axon collaterals stimulates granule cells via AMPA/kainate and NMDA receptors. Granule cells release GABA back onto GABAA receptors on the same and other mitral cells. Glutamate release from a mitral cell can therefore cause recurrent inhibition of the same mitral cell and lateral inhibition of other mitral cells via periglomerular and granule cells. These interactions, here collectively referred to as the mitral cell→interneuron→mitral cell pathway, can extend over distances corresponding to multiple glomeruli. An additional pathway mediating lateral inhibition that is not detailed in this scheme is the short axon cell (SAC)→periglomerular→mitral cell pathway identified in rodents [13], [54]. Centrifugal inputs from higher brain areas are also not shown in detail. Many of these inputs terminate on interneurons and are glutamatergic. Not included in the scheme are metabotropic glutamate receptors, interactions among interneurons in the granule cell layer [55], glutamate spillover [56], and a small glutamatergic subpopulation of granule cells [57]. Strong excitatory interactions across glomeruli, as revealed in the antennal lobe of Drosophila [58]–[60], have not been found in the vertebrate olfactory bulb. Abbreviations: OSN: olfactory sensory neuron, PGC: periglomerular cell, MC: mitral cell, GC: granule cell, SAC: short axon cell.

Mentions: The synaptic architecture of neuronal circuits in the olfactory bulb is conserved across vertebrate classes [7], [8]. Within the sensory input modules of the olfactory bulb, the glomeruli, mitral cells can excite one another via gap junctions and fast volume transmission of glutamate [9]–[12]. Across glomeruli, synaptic interactions are mediated by interneurons, predominantly periglomerular and granule cells. Interactions among neurons associated with different glomeruli occur via various synaptic pathways that extend over multiple spatial scales and exert predominantly inhibitory effects on olfactory bulb output neurons [13], [14] (Fig. 1). The most prominent inter-glomerular synaptic pathway is the mitral cell→interneuron→mitral cell pathway, where periglomerular or granule cells are excited by glutamatergic mitral cell→interneuron synapses and feed back GABAergic inhibition onto the same and other mitral cells at interneuron→mitral cell synapses. This and other pathways (Fig. 1) shape spatio-temporal patterns of olfactory bulb output activity and may thereby optimize odor representations for processing in higher brain regions.


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

Tabor R, Friedrich RW - PLoS ONE (2008)

Simplified architecture of synaptic pathways in the olfactory bulb.Within glomeruli, glutamatergic olfactory sensory neurons provide excitatory synaptic input to mitral cells and a subpopulation of periglomerular cells via AMPA/kainate and NMDA receptors. Periglomerular cells also receive glutamatergic input from mitral cell dendrites and provide GABAergic output to mitral cells of the same and neighbouring glomeruli. In addition, GABA (green arrow) and dopamine (not shown) released from periglomerular cells reduces glutamate release from olfactory sensory neuron axon terminals by acting on GABAB and D2 receptors, respectively, in the same glomerulus [23], [49]–[53]. In subglomerular layers, glutamate release from mitral cell dendrites and axon collaterals stimulates granule cells via AMPA/kainate and NMDA receptors. Granule cells release GABA back onto GABAA receptors on the same and other mitral cells. Glutamate release from a mitral cell can therefore cause recurrent inhibition of the same mitral cell and lateral inhibition of other mitral cells via periglomerular and granule cells. These interactions, here collectively referred to as the mitral cell→interneuron→mitral cell pathway, can extend over distances corresponding to multiple glomeruli. An additional pathway mediating lateral inhibition that is not detailed in this scheme is the short axon cell (SAC)→periglomerular→mitral cell pathway identified in rodents [13], [54]. Centrifugal inputs from higher brain areas are also not shown in detail. Many of these inputs terminate on interneurons and are glutamatergic. Not included in the scheme are metabotropic glutamate receptors, interactions among interneurons in the granule cell layer [55], glutamate spillover [56], and a small glutamatergic subpopulation of granule cells [57]. Strong excitatory interactions across glomeruli, as revealed in the antennal lobe of Drosophila [58]–[60], have not been found in the vertebrate olfactory bulb. Abbreviations: OSN: olfactory sensory neuron, PGC: periglomerular cell, MC: mitral cell, GC: granule cell, SAC: short axon cell.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2169298&req=5

pone-0001416-g001: Simplified architecture of synaptic pathways in the olfactory bulb.Within glomeruli, glutamatergic olfactory sensory neurons provide excitatory synaptic input to mitral cells and a subpopulation of periglomerular cells via AMPA/kainate and NMDA receptors. Periglomerular cells also receive glutamatergic input from mitral cell dendrites and provide GABAergic output to mitral cells of the same and neighbouring glomeruli. In addition, GABA (green arrow) and dopamine (not shown) released from periglomerular cells reduces glutamate release from olfactory sensory neuron axon terminals by acting on GABAB and D2 receptors, respectively, in the same glomerulus [23], [49]–[53]. In subglomerular layers, glutamate release from mitral cell dendrites and axon collaterals stimulates granule cells via AMPA/kainate and NMDA receptors. Granule cells release GABA back onto GABAA receptors on the same and other mitral cells. Glutamate release from a mitral cell can therefore cause recurrent inhibition of the same mitral cell and lateral inhibition of other mitral cells via periglomerular and granule cells. These interactions, here collectively referred to as the mitral cell→interneuron→mitral cell pathway, can extend over distances corresponding to multiple glomeruli. An additional pathway mediating lateral inhibition that is not detailed in this scheme is the short axon cell (SAC)→periglomerular→mitral cell pathway identified in rodents [13], [54]. Centrifugal inputs from higher brain areas are also not shown in detail. Many of these inputs terminate on interneurons and are glutamatergic. Not included in the scheme are metabotropic glutamate receptors, interactions among interneurons in the granule cell layer [55], glutamate spillover [56], and a small glutamatergic subpopulation of granule cells [57]. Strong excitatory interactions across glomeruli, as revealed in the antennal lobe of Drosophila [58]–[60], have not been found in the vertebrate olfactory bulb. Abbreviations: OSN: olfactory sensory neuron, PGC: periglomerular cell, MC: mitral cell, GC: granule cell, SAC: short axon cell.
Mentions: The synaptic architecture of neuronal circuits in the olfactory bulb is conserved across vertebrate classes [7], [8]. Within the sensory input modules of the olfactory bulb, the glomeruli, mitral cells can excite one another via gap junctions and fast volume transmission of glutamate [9]–[12]. Across glomeruli, synaptic interactions are mediated by interneurons, predominantly periglomerular and granule cells. Interactions among neurons associated with different glomeruli occur via various synaptic pathways that extend over multiple spatial scales and exert predominantly inhibitory effects on olfactory bulb output neurons [13], [14] (Fig. 1). The most prominent inter-glomerular synaptic pathway is the mitral cell→interneuron→mitral cell pathway, where periglomerular or granule cells are excited by glutamatergic mitral cell→interneuron synapses and feed back GABAergic inhibition onto the same and other mitral cells at interneuron→mitral cell synapses. This and other pathways (Fig. 1) shape spatio-temporal patterns of olfactory bulb output activity and may thereby optimize odor representations for processing in higher brain regions.

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