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Topological reorganization of odor representations in the olfactory bulb.

Yaksi E, Judkewitz B, Friedrich RW - PLoS Biol. (2007)

Bottom Line: Shortly after response onset, activity patterns exhibited foci of activity associated with certain chemical features throughout all layers.Nevertheless, transient chemotopic maps may support neuronal computations by establishing important synaptic interactions within the circuit.These results provide insights into the functional topology of neural activity patterns and its potential role in circuit function.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Optics, Max-Planck-Institute for Medical Research, Heidelberg, Germany.

ABSTRACT
Odors are initially represented in the olfactory bulb (OB) by patterns of sensory input across the array of glomeruli. Although activated glomeruli are often widely distributed, glomeruli responding to stimuli sharing molecular features tend to be loosely clustered and thus establish a fractured chemotopic map. Neuronal circuits in the OB transform glomerular patterns of sensory input into spatiotemporal patterns of output activity and thereby extract information about a stimulus. It is, however, unknown whether the chemotopic spatial organization of glomerular inputs is maintained during these computations. To explore this issue, we measured spatiotemporal patterns of odor-evoked activity across thousands of individual neurons in the zebrafish OB by temporally deconvolved two-photon Ca(2+) imaging. Mitral cells and interneurons were distinguished by transgenic markers and exhibited different response selectivities. Shortly after response onset, activity patterns exhibited foci of activity associated with certain chemical features throughout all layers. During the subsequent few hundred milliseconds, however, MC activity was locally sparsened within the initial foci in an odor-specific manner. As a consequence, chemotopic maps disappeared and activity patterns became more informative about precise odor identity. Hence, chemotopic maps of glomerular input activity are initially transmitted to OB outputs, but not maintained during pattern processing. Nevertheless, transient chemotopic maps may support neuronal computations by establishing important synaptic interactions within the circuit. These results provide insights into the functional topology of neural activity patterns and its potential role in circuit function.

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Comparison of Three-Dimensional IN Activity Patterns(A) Overlay of IN response patterns evoked by chemically related odors (Trp and Tyr) in successive 256-ms time windows (same as in Figure 5B; n = 1,612 INs). Conventions as in Figure 7A. Sphere size depicts TDCa signal between 2 and 10 (arbitrary units); dots depict INs with TDCa signals less than 2. Distance between ticks is 50 μm on all axes. Orientation is as indicated: anterior to posterior (A–P), medial to lateral (M–L), and dorsal to ventral (D–V).(B) Overlay of IN response patterns evoked by two dissimilar stimuli. Same conventions as in (A).
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pbio-0050178-g008: Comparison of Three-Dimensional IN Activity Patterns(A) Overlay of IN response patterns evoked by chemically related odors (Trp and Tyr) in successive 256-ms time windows (same as in Figure 5B; n = 1,612 INs). Conventions as in Figure 7A. Sphere size depicts TDCa signal between 2 and 10 (arbitrary units); dots depict INs with TDCa signals less than 2. Distance between ticks is 50 μm on all axes. Orientation is as indicated: anterior to posterior (A–P), medial to lateral (M–L), and dorsal to ventral (D–V).(B) Overlay of IN response patterns evoked by two dissimilar stimuli. Same conventions as in (A).

Mentions: Overlays of IN activity patterns evoked by chemically similar stimuli (e.g., Lys and Arg) showed little or no reduction in the overlap during the initial phase of the odor response (Figure 8A), consistent with the observation that correlations between IN activity patterns remain high during the decorrelation of MC activity patterns (Figure 3A and 3B). The overlap between IN activity patterns evoked by dissimilar stimuli (e.g., Lys and Tyr) was lower but still substantial (Figure 8B). These observations are consistent with results from correlation analysis (Figure 3A).


Topological reorganization of odor representations in the olfactory bulb.

Yaksi E, Judkewitz B, Friedrich RW - PLoS Biol. (2007)

Comparison of Three-Dimensional IN Activity Patterns(A) Overlay of IN response patterns evoked by chemically related odors (Trp and Tyr) in successive 256-ms time windows (same as in Figure 5B; n = 1,612 INs). Conventions as in Figure 7A. Sphere size depicts TDCa signal between 2 and 10 (arbitrary units); dots depict INs with TDCa signals less than 2. Distance between ticks is 50 μm on all axes. Orientation is as indicated: anterior to posterior (A–P), medial to lateral (M–L), and dorsal to ventral (D–V).(B) Overlay of IN response patterns evoked by two dissimilar stimuli. Same conventions as in (A).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1904499&req=5

pbio-0050178-g008: Comparison of Three-Dimensional IN Activity Patterns(A) Overlay of IN response patterns evoked by chemically related odors (Trp and Tyr) in successive 256-ms time windows (same as in Figure 5B; n = 1,612 INs). Conventions as in Figure 7A. Sphere size depicts TDCa signal between 2 and 10 (arbitrary units); dots depict INs with TDCa signals less than 2. Distance between ticks is 50 μm on all axes. Orientation is as indicated: anterior to posterior (A–P), medial to lateral (M–L), and dorsal to ventral (D–V).(B) Overlay of IN response patterns evoked by two dissimilar stimuli. Same conventions as in (A).
Mentions: Overlays of IN activity patterns evoked by chemically similar stimuli (e.g., Lys and Arg) showed little or no reduction in the overlap during the initial phase of the odor response (Figure 8A), consistent with the observation that correlations between IN activity patterns remain high during the decorrelation of MC activity patterns (Figure 3A and 3B). The overlap between IN activity patterns evoked by dissimilar stimuli (e.g., Lys and Tyr) was lower but still substantial (Figure 8B). These observations are consistent with results from correlation analysis (Figure 3A).

Bottom Line: Shortly after response onset, activity patterns exhibited foci of activity associated with certain chemical features throughout all layers.Nevertheless, transient chemotopic maps may support neuronal computations by establishing important synaptic interactions within the circuit.These results provide insights into the functional topology of neural activity patterns and its potential role in circuit function.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Optics, Max-Planck-Institute for Medical Research, Heidelberg, Germany.

ABSTRACT
Odors are initially represented in the olfactory bulb (OB) by patterns of sensory input across the array of glomeruli. Although activated glomeruli are often widely distributed, glomeruli responding to stimuli sharing molecular features tend to be loosely clustered and thus establish a fractured chemotopic map. Neuronal circuits in the OB transform glomerular patterns of sensory input into spatiotemporal patterns of output activity and thereby extract information about a stimulus. It is, however, unknown whether the chemotopic spatial organization of glomerular inputs is maintained during these computations. To explore this issue, we measured spatiotemporal patterns of odor-evoked activity across thousands of individual neurons in the zebrafish OB by temporally deconvolved two-photon Ca(2+) imaging. Mitral cells and interneurons were distinguished by transgenic markers and exhibited different response selectivities. Shortly after response onset, activity patterns exhibited foci of activity associated with certain chemical features throughout all layers. During the subsequent few hundred milliseconds, however, MC activity was locally sparsened within the initial foci in an odor-specific manner. As a consequence, chemotopic maps disappeared and activity patterns became more informative about precise odor identity. Hence, chemotopic maps of glomerular input activity are initially transmitted to OB outputs, but not maintained during pattern processing. Nevertheless, transient chemotopic maps may support neuronal computations by establishing important synaptic interactions within the circuit. These results provide insights into the functional topology of neural activity patterns and its potential role in circuit function.

Show MeSH
Related in: MedlinePlus