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Transformation of odor representations in target areas of the olfactory bulb

Abstract

The brain generates coherent perceptions of objects from elementary sensory inputs. To examine how higher-order representations of smells arise from the activation of discrete combinations of glomeruli, we analyzed transformations of activity patterns between the zebrafish olfactory bulb and two of its telencephalic targets, Vv and Dp. Vv is subpallial whereas Dp is the homolog of olfactory cortex. Both areas lack an obvious topographic organization but perform complementary computations. Responses to different odors and their mixtures indicate that Vv neurons pool convergent inputs, resulting in broadened tuning curves and overlapping odor representations. Neuronal circuits in Dp, in contrast, produce a mixture of excitatory and inhibitory synaptic inputs to each neuron that controls action potential firing in an odor-dependent manner. This mechanism can extract information about combinations of molecular features from ensembles of active and inactive mitral cells, suggesting that pattern processing in Dp establishes representations of odor objects.

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Figure 1: Odor responses in target areas of the olfactory bulb.
Figure 2: Three-dimensional activity patterns across mitral cells and interneurons (INs) in the olfactory bulb.
Figure 3: Three-dimensional activity patterns in Vv and Dp.
Figure 4: Topological organization and response properties of neurons in different brain areas.
Figure 5: Mixture interactions.
Figure 6: Inhibitory control of action potential initiation in Dp neurons.

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Acknowledgements

We thank P. Caroni, T. Oertner, B. Roska and members of the Friedrich laboratory, particularly M. Wiechert, for stimulating discussions and comments on the manuscript. We are grateful to W. Denk for support. This work was supported by the Novartis Research Foundation, the Max Planck Society, the Deutsche Forschungsgemeinschaft (GK 791; SFBs 488, 780; FOR 643), the Minna-James-Heineman Foundation and the Boehringer Ingelheim Fonds (to E.Y. and S.T.B.).

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E.Y. performed widefield imaging experiments, measured three-dimensional activity patterns and performed analyses of three-dimensional activity patterns and single-neuron responses; F.v.S.P. measured responses to binary mixtures, performed pharmacological experiments and electrophysiological recordings, and analyzed the data; J.N. measured responses to binary mixtures; S.T.B. participated in the construction of imaging and odor stimulation equipment and helped with experiments; R.W.F. is the principal investigator, conceived the study, constructed equipment, performed some of the binary mixture experiments, contributed to the data analysis and wrote the manuscript.

Corresponding author

Correspondence to Rainer W Friedrich.

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Yaksi, E., von Saint Paul, F., Niessing, J. et al. Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 12, 474–482 (2009). https://doi.org/10.1038/nn.2288

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