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Nasal chemosensory-stimulation evoked activity patterns in the rat trigeminal ganglion visualized by in vivo voltage-sensitive dye imaging.

Rothermel M, Ng BS, Grabska-Barwińska A, Hatt H, Jancke D - PLoS ONE (2011)

Bottom Line: Mammalian nasal chemosensation is predominantly mediated by two independent neuronal pathways, the olfactory and the trigeminal system.Within the early olfactory system, spatiotemporal responses of the olfactory bulb to various odorants have been mapped in great detail.Application of different chemical stimuli to the nasal cavity elicited distinct, stimulus-category specific, spatiotemporal activation patterns that comprised activated as well as suppressed areas.

View Article: PubMed Central - PubMed

Affiliation: Lehrstuhl für Zellphysiologie, Ruhr-Universität, Bochum, Germany.

ABSTRACT
Mammalian nasal chemosensation is predominantly mediated by two independent neuronal pathways, the olfactory and the trigeminal system. Within the early olfactory system, spatiotemporal responses of the olfactory bulb to various odorants have been mapped in great detail. In contrast, far less is known about the representation of volatile chemical stimuli at an early stage in the trigeminal system, the trigeminal ganglion (TG), which contains neurons directly projecting to the nasal cavity. We have established an in vivo preparation that allows high-resolution imaging of neuronal population activity from a large region of the rat TG using voltage-sensitive dyes (VSDs). Application of different chemical stimuli to the nasal cavity elicited distinct, stimulus-category specific, spatiotemporal activation patterns that comprised activated as well as suppressed areas. Thus, our results provide the first direct insights into the spatial representation of nasal chemosensory information within the trigeminal ganglion imaged at high temporal resolution.

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In vivo VSD recording of the rat TG.(A) Trigeminal VSD activation pattern elicited by nasal ethanol application (z-score map, mean over 2,8 s). Arrow and arrowhead point to activated areas in the near-posterior, central-lateral and anterior trigeminal region, respectively; scale bar, 1 mm; P, posterior; L, lateral (B) Correlation of activity patterns to the location of nasal trigeminal neurons: Major clusters of nasal trigeminal neurons could be identified in the near-posterior, central-lateral region as well as in an anterior region on both sides relative to the midline of the ganglion (color code = number of animals showing infected cells at identical trigeminal regions). Arrows point to commonly activated area in CO2 and ethanol conditions; arrowheads to unique ethanol activity in VSD measurements (compare Figure 3A). Black trace = schematic TG outline; scale bar, 1 mm; Inserts: Representative fluorescence images showing traced nasal trigeminal neurons; scale bar, 20 µm.
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pone-0026158-g002: In vivo VSD recording of the rat TG.(A) Trigeminal VSD activation pattern elicited by nasal ethanol application (z-score map, mean over 2,8 s). Arrow and arrowhead point to activated areas in the near-posterior, central-lateral and anterior trigeminal region, respectively; scale bar, 1 mm; P, posterior; L, lateral (B) Correlation of activity patterns to the location of nasal trigeminal neurons: Major clusters of nasal trigeminal neurons could be identified in the near-posterior, central-lateral region as well as in an anterior region on both sides relative to the midline of the ganglion (color code = number of animals showing infected cells at identical trigeminal regions). Arrows point to commonly activated area in CO2 and ethanol conditions; arrowheads to unique ethanol activity in VSD measurements (compare Figure 3A). Black trace = schematic TG outline; scale bar, 1 mm; Inserts: Representative fluorescence images showing traced nasal trigeminal neurons; scale bar, 20 µm.

Mentions: For spatial analysis of the evoked activity, we averaged recordings across trials and time. The evoked patterns were then expressed in z-score. Such a statistical activation map derived from a different subject is presented in Figure 2A. Activated areas include regions in the near-posterior, central to lateral and anterior ganglion together with suppression in posterior trigeminal areas. Changing the stimulus application site altered this spatial layout: when ethanol was applied instead to the oral cavity, a region in the anterior-medial ganglion became predominantly activated (asterisk Figure S2), suggesting minimal (if any) contribution of oral activation to the activation pattern evoked by nasal application of ethanol.


Nasal chemosensory-stimulation evoked activity patterns in the rat trigeminal ganglion visualized by in vivo voltage-sensitive dye imaging.

Rothermel M, Ng BS, Grabska-Barwińska A, Hatt H, Jancke D - PLoS ONE (2011)

In vivo VSD recording of the rat TG.(A) Trigeminal VSD activation pattern elicited by nasal ethanol application (z-score map, mean over 2,8 s). Arrow and arrowhead point to activated areas in the near-posterior, central-lateral and anterior trigeminal region, respectively; scale bar, 1 mm; P, posterior; L, lateral (B) Correlation of activity patterns to the location of nasal trigeminal neurons: Major clusters of nasal trigeminal neurons could be identified in the near-posterior, central-lateral region as well as in an anterior region on both sides relative to the midline of the ganglion (color code = number of animals showing infected cells at identical trigeminal regions). Arrows point to commonly activated area in CO2 and ethanol conditions; arrowheads to unique ethanol activity in VSD measurements (compare Figure 3A). Black trace = schematic TG outline; scale bar, 1 mm; Inserts: Representative fluorescence images showing traced nasal trigeminal neurons; scale bar, 20 µm.
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Related In: Results  -  Collection

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pone-0026158-g002: In vivo VSD recording of the rat TG.(A) Trigeminal VSD activation pattern elicited by nasal ethanol application (z-score map, mean over 2,8 s). Arrow and arrowhead point to activated areas in the near-posterior, central-lateral and anterior trigeminal region, respectively; scale bar, 1 mm; P, posterior; L, lateral (B) Correlation of activity patterns to the location of nasal trigeminal neurons: Major clusters of nasal trigeminal neurons could be identified in the near-posterior, central-lateral region as well as in an anterior region on both sides relative to the midline of the ganglion (color code = number of animals showing infected cells at identical trigeminal regions). Arrows point to commonly activated area in CO2 and ethanol conditions; arrowheads to unique ethanol activity in VSD measurements (compare Figure 3A). Black trace = schematic TG outline; scale bar, 1 mm; Inserts: Representative fluorescence images showing traced nasal trigeminal neurons; scale bar, 20 µm.
Mentions: For spatial analysis of the evoked activity, we averaged recordings across trials and time. The evoked patterns were then expressed in z-score. Such a statistical activation map derived from a different subject is presented in Figure 2A. Activated areas include regions in the near-posterior, central to lateral and anterior ganglion together with suppression in posterior trigeminal areas. Changing the stimulus application site altered this spatial layout: when ethanol was applied instead to the oral cavity, a region in the anterior-medial ganglion became predominantly activated (asterisk Figure S2), suggesting minimal (if any) contribution of oral activation to the activation pattern evoked by nasal application of ethanol.

Bottom Line: Mammalian nasal chemosensation is predominantly mediated by two independent neuronal pathways, the olfactory and the trigeminal system.Within the early olfactory system, spatiotemporal responses of the olfactory bulb to various odorants have been mapped in great detail.Application of different chemical stimuli to the nasal cavity elicited distinct, stimulus-category specific, spatiotemporal activation patterns that comprised activated as well as suppressed areas.

View Article: PubMed Central - PubMed

Affiliation: Lehrstuhl für Zellphysiologie, Ruhr-Universität, Bochum, Germany.

ABSTRACT
Mammalian nasal chemosensation is predominantly mediated by two independent neuronal pathways, the olfactory and the trigeminal system. Within the early olfactory system, spatiotemporal responses of the olfactory bulb to various odorants have been mapped in great detail. In contrast, far less is known about the representation of volatile chemical stimuli at an early stage in the trigeminal system, the trigeminal ganglion (TG), which contains neurons directly projecting to the nasal cavity. We have established an in vivo preparation that allows high-resolution imaging of neuronal population activity from a large region of the rat TG using voltage-sensitive dyes (VSDs). Application of different chemical stimuli to the nasal cavity elicited distinct, stimulus-category specific, spatiotemporal activation patterns that comprised activated as well as suppressed areas. Thus, our results provide the first direct insights into the spatial representation of nasal chemosensory information within the trigeminal ganglion imaged at high temporal resolution.

Show MeSH
Related in: MedlinePlus