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J Neurophysiol 102: 817-830, 2009. First published May 27, 2009; doi:10.1152/jn.00020.2009
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Optical Imaging of Postsynaptic Odor Representation in the Glomerular Layer of the Mouse Olfactory Bulb

Max L. Fletcher1,3, Arjun V. Masurkar1, Junling Xing1, Fumiaki Imamura4, Wenhui Xiong1,3, Shin Nagayama1,3, Hiroki Mutoh2, Charles A. Greer1,4, Thomas Knöpfel2 and Wei R. Chen1,3

1Departments of Neurobiology and 4Neurosurgery, Yale University School of Medicine, New Haven, Connecticut; 2Laboratory for Neuronal Circuit Dynamics, RIKEN Brain Science Institute, Wako-shi, Japan; and 3Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas

Submitted 8 January 2009; accepted in final form 11 May 2009

Olfactory glomeruli are the loci where the first odor-representation map emerges. The glomerular layer comprises exquisite local synaptic circuits for the processing of olfactory coding patterns immediately after their emergence. To understand how an odor map is transferred from afferent terminals to postsynaptic dendrites, it is essential to directly monitor the odor-evoked glomerular postsynaptic activity patterns. Here we report the use of a transgenic mouse expressing a Ca2+-sensitive green fluorescence protein (GCaMP2) under a Kv3.1 potassium-channel promoter. Immunostaining revealed that GCaMP2 was specifically expressed in mitral and tufted cells and a subpopulation of juxtaglomerular cells but not in olfactory nerve terminals. Both in vitro and in vivo imaging combined with glutamate receptor pharmacology confirmed that odor maps reported by GCaMP2 were of a postsynaptic origin. These mice thus provided an unprecedented opportunity to analyze the spatial activity pattern reflecting purely postsynaptic olfactory codes. The odor-evoked GCaMP2 signal had both focal and diffuse spatial components. The focalized hot spots corresponded to individually activated glomeruli. In GCaMP2-reported postsynaptic odor maps, different odorants activated distinct but overlapping sets of glomeruli. Increasing odor concentration increased both individual glomerular response amplitude and the total number of activated glomeruli. Furthermore, the GCaMP2 response displayed a fast time course that enabled us to analyze the temporal dynamics of odor maps over consecutive sniff cycles. In summary, with cell-specific targeting of a genetically encoded Ca2+ indicator, we have successfully isolated and characterized an intermediate level of odor representation between olfactory nerve input and principal mitral/tufted cell output.

Address for reprint requests and other correspondence: M. L. Fletcher, University of Texas Medical School, Dept. of Neurobiology and Anatomy, 6431 Fannin St., Suite MSB 7.046 Houston, TX 77030 (E-mail: max.fletcher{at}uth.tmc.edu)






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