Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb

Max L. Fletcher, Arjun V. Masurkar, Junling Xing, Fumiaki Imamura, Wenhui Xiong, Shin Nagayama, Hiroki Mutoh, Charles A. Greer, Thomas Knöpfel, Wei R. Chen

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

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 Ca 2+ -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 Ca 2+ indicator, we have successfully isolated and characterized an intermediate level of odor representation between olfactory nerve input and principal mitral/tufted cell output.

Original languageEnglish (US)
Pages (from-to)817-830
Number of pages14
JournalJournal of Neurophysiology
Volume102
Issue number2
DOIs
StatePublished - Aug 1 2009

Fingerprint

Olfactory Bulb
Optical Imaging
Olfactory Nerve
Shaw Potassium Channels
Odorants
Spatial Analysis
Glutamate Receptors
Dendrites
Transgenic Mice
Fluorescence
Pharmacology

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

Fletcher, Max L. ; Masurkar, Arjun V. ; Xing, Junling ; Imamura, Fumiaki ; Xiong, Wenhui ; Nagayama, Shin ; Mutoh, Hiroki ; Greer, Charles A. ; Knöpfel, Thomas ; Chen, Wei R. / Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb. In: Journal of Neurophysiology. 2009 ; Vol. 102, No. 2. pp. 817-830.
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Fletcher, ML, Masurkar, AV, Xing, J, Imamura, F, Xiong, W, Nagayama, S, Mutoh, H, Greer, CA, Knöpfel, T & Chen, WR 2009, 'Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb', Journal of Neurophysiology, vol. 102, no. 2, pp. 817-830. https://doi.org/10.1152/jn.00020.2009

Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb. / Fletcher, Max L.; Masurkar, Arjun V.; Xing, Junling; Imamura, Fumiaki; Xiong, Wenhui; Nagayama, Shin; Mutoh, Hiroki; Greer, Charles A.; Knöpfel, Thomas; Chen, Wei R.

In: Journal of Neurophysiology, Vol. 102, No. 2, 01.08.2009, p. 817-830.

Research output: Contribution to journalArticle

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T1 - Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb

AU - Fletcher, Max L.

AU - Masurkar, Arjun V.

AU - Xing, Junling

AU - Imamura, Fumiaki

AU - Xiong, Wenhui

AU - Nagayama, Shin

AU - Mutoh, Hiroki

AU - Greer, Charles A.

AU - Knöpfel, Thomas

AU - Chen, Wei R.

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AB - 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 Ca 2+ -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 Ca 2+ indicator, we have successfully isolated and characterized an intermediate level of odor representation between olfactory nerve input and principal mitral/tufted cell output.

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