Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse

Abstract

Sensory inputs frequently converge on the brain in a spatially organized manner, often with overlapping inputs to multiple target neurons. Whether the responses of target neurons with common inputs become decorrelated depends on the contribution of local circuit interactions. We addressed this issue in the olfactory system using newly generated transgenic mice that express channelrhodopsin-2 in all of the olfactory sensory neurons. By selectively stimulating individual glomeruli with light, we identified mitral/tufted cells that receive common input (sister cells). Sister cells had highly correlated responses to odors, as measured by average spike rates, but their spike timing in relation to respiration was differentially altered. In contrast, non-sister cells correlated poorly on both of these measures. We suggest that sister mitral/tufted cells carry two different channels of information: average activity representing shared glomerular input and phase-specific information that refines odor representations and is substantially independent for sister cells.

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Figure 1: ORC transgenic expression pattern.
Figure 2: DMD patterned illumination in ORC mice maps the parent glomeruli of mitral/tufted cells in vivo.
Figure 3: Functional hotspots correspond to anatomically identified glomeruli.
Figure 4: Light mapping sorts mitral/tufted cells into sister and non-sister pairs.
Figure 5: Examples of similarities and differences in odor responses of sister mitral/tufted cells.
Figure 6: Sister mitral/tufted cells have correlated changes in odor induced firing rates.
Figure 7: Odors disrupt phase correlations of sister and non-sister mitral/tufted cells.
Figure 8: Odors trigger firing rate and phase changes in an independent manner.

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Acknowledgements

We thank the Genome Manipulation Facility at Harvard University for help with generating the ORC mice. We are grateful to M. Meister, A. Kepecs, G. Turner, A. Khan, S. Kumari and P. Gupta for comments on the manuscript. B. Burbach, H. Cho, R. Eifert and M. Davis provided excellent technical support. We thank G. Otazu and S. Ranade for advice on building tetrodes and H. Oviedo and A. Zador for access to the laser-scanning photostimulation rig. Our special thanks go to Megabus for swift transportation and to the House of Marks. A.K.D. and D.F.A. were supported by the Cold Spring Harbor Laboratory Fellows Program. Additional support for A.K.D. was provided by the International Society for Neurochemistry, Sarojini Damodaran fellowship (Tata Institute of Fundamental Research) and Merck.

Author information

A.K.D. and D.F.A. designed the study. D.F.A. engineered the ORC transgenic mice in the laboratory of V.N.M. A.H. characterized the expression pattern of ORC mice and performed acute slice recordings. A.K.D. and D.F.A. built the DLP stimulation rig and performed in vivo experiments. A.K.D. wrote custom software for recording and analysis. A.K.D. and D.F.A. analyzed the data. U.S.B. and V.N.M. provided expert advice on data analysis and guidance with experimental design. A.K.D., U.S.B., V.N.M. and D.F.A. wrote the manuscript.

Correspondence to Venkatesh N Murthy or Dinu F Albeanu.

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Dhawale, A., Hagiwara, A., Bhalla, U. et al. Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci 13, 1404–1412 (2010). https://doi.org/10.1038/nn.2673

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