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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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Spatiotemporal dynamics of trigeminal responses in a single trial.(A) Schematic view demonstrating TG location at the base of the skull (after decerebration). Bottom: Illustration of the skull-base anatomy (modified from [44]). TG is marked in orange. Top: TG vascular image; scale bar = 1 mm; dotted black line = animal midline; man, mandibular branch; on, optic nerve; oph-max, ophthalmomaxillary branch. (B) Timecourse of VSD activity in the TG following nasal application of ethanol. 0 ms denotes stimulus onset. Each frame represents 10 ms of recording extracted from the original timecourse at regular time points (frames of interest are represented in higher temporal resolution). Coordinated activation of the trigeminal ganglion occurred in brief repeated pulses of variable duration and at variable intervals. White bar = 1 mm.
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pone-0026158-g001: Spatiotemporal dynamics of trigeminal responses in a single trial.(A) Schematic view demonstrating TG location at the base of the skull (after decerebration). Bottom: Illustration of the skull-base anatomy (modified from [44]). TG is marked in orange. Top: TG vascular image; scale bar = 1 mm; dotted black line = animal midline; man, mandibular branch; on, optic nerve; oph-max, ophthalmomaxillary branch. (B) Timecourse of VSD activity in the TG following nasal application of ethanol. 0 ms denotes stimulus onset. Each frame represents 10 ms of recording extracted from the original timecourse at regular time points (frames of interest are represented in higher temporal resolution). Coordinated activation of the trigeminal ganglion occurred in brief repeated pulses of variable duration and at variable intervals. White bar = 1 mm.

Mentions: Anesthesia was induced with Chloralhydrate (i.p., 4% solution in saline, 400 mg kg−1). Lidocaine (1%, s.c.) was applied to all pressure points and incisions. Immediately before fixation in the stereotactic device, subjects were reverse-tracheotomized (also known as a double tracheotomy, as adapted from an earlier study [6]). In this procedure, two separated tubes were placed into each trachea opening created by a single incision. Subjects were artificially ventilated through the lower tracheotomy tube leading to the lungs (50–70 cycles/min, 4–6 ml tidal volume; UGO BASILE, Italy), while the upper tracheotomy tube allowed for the control of a smooth, constant through-passage of the stimulation air stream. Anesthesia was maintained using isoflurane (1–1,5%). Electrocardiogram and rectal temperature were continuously monitored (core temperature was held at 37.5°C). A craniotomy was performed to expose the cerebral hemispheres, which were then gently aspirated to gain access to the trigeminal ganglia at the base of the skull (Figure 1A). After decerebration (which caused unconsciousness) isoflurane was decreased to less than 1% (to rule out influences on nociceptive ion channels). Preparations were stable up to 24 hours. After the experiments rats were euthanized with an overdose of anesthetic.


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)

Spatiotemporal dynamics of trigeminal responses in a single trial.(A) Schematic view demonstrating TG location at the base of the skull (after decerebration). Bottom: Illustration of the skull-base anatomy (modified from [44]). TG is marked in orange. Top: TG vascular image; scale bar = 1 mm; dotted black line = animal midline; man, mandibular branch; on, optic nerve; oph-max, ophthalmomaxillary branch. (B) Timecourse of VSD activity in the TG following nasal application of ethanol. 0 ms denotes stimulus onset. Each frame represents 10 ms of recording extracted from the original timecourse at regular time points (frames of interest are represented in higher temporal resolution). Coordinated activation of the trigeminal ganglion occurred in brief repeated pulses of variable duration and at variable intervals. White bar = 1 mm.
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Related In: Results  -  Collection

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pone-0026158-g001: Spatiotemporal dynamics of trigeminal responses in a single trial.(A) Schematic view demonstrating TG location at the base of the skull (after decerebration). Bottom: Illustration of the skull-base anatomy (modified from [44]). TG is marked in orange. Top: TG vascular image; scale bar = 1 mm; dotted black line = animal midline; man, mandibular branch; on, optic nerve; oph-max, ophthalmomaxillary branch. (B) Timecourse of VSD activity in the TG following nasal application of ethanol. 0 ms denotes stimulus onset. Each frame represents 10 ms of recording extracted from the original timecourse at regular time points (frames of interest are represented in higher temporal resolution). Coordinated activation of the trigeminal ganglion occurred in brief repeated pulses of variable duration and at variable intervals. White bar = 1 mm.
Mentions: Anesthesia was induced with Chloralhydrate (i.p., 4% solution in saline, 400 mg kg−1). Lidocaine (1%, s.c.) was applied to all pressure points and incisions. Immediately before fixation in the stereotactic device, subjects were reverse-tracheotomized (also known as a double tracheotomy, as adapted from an earlier study [6]). In this procedure, two separated tubes were placed into each trachea opening created by a single incision. Subjects were artificially ventilated through the lower tracheotomy tube leading to the lungs (50–70 cycles/min, 4–6 ml tidal volume; UGO BASILE, Italy), while the upper tracheotomy tube allowed for the control of a smooth, constant through-passage of the stimulation air stream. Anesthesia was maintained using isoflurane (1–1,5%). Electrocardiogram and rectal temperature were continuously monitored (core temperature was held at 37.5°C). A craniotomy was performed to expose the cerebral hemispheres, which were then gently aspirated to gain access to the trigeminal ganglia at the base of the skull (Figure 1A). After decerebration (which caused unconsciousness) isoflurane was decreased to less than 1% (to rule out influences on nociceptive ion channels). Preparations were stable up to 24 hours. After the experiments rats were euthanized with an overdose of anesthetic.

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