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Eyelid Opening with Trigeminal Proprioceptive Activation Regulates a Brainstem Arousal Mechanism.

Matsuo K, Ban R, Hama Y, Yuzuriha S - PLoS ONE (2015)

Bottom Line: Upgaze phasically and degree-dependently increased deoxyhemoglobin level at Fp1 and Fp2, whereas downgaze phasically decreased it in 16 subjects.Unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle used to significantly reduce trigeminal proprioceptive evocation ipsilaterally impaired the increased deoxyhemoglobin level by 60° upgaze at Fp1 or Fp2 in 6 subjects.We concluded that upgaze with strong trigeminal proprioceptive evocation was sufficient to phasically activate sympathetically innervated sweat glands and appeared to induce rapid oxygen consumption in the ventromedial prefrontal cortex and to rapidly produce deoxyhemoglobin to regulate physiological arousal.

View Article: PubMed Central - PubMed

Affiliation: Department of Plastic and Reconstructive Surgery, Shinshu University School of Medicine, Matsumoto, Japan.

ABSTRACT
Eyelid opening stretches mechanoreceptors in the supratarsal Müller muscle to activate the proprioceptive fiber supplied by the trigeminal mesencephalic nucleus. This proprioception induces reflex contractions of the slow-twitch fibers in the levator palpebrae superioris and frontalis muscles to sustain eyelid and eyebrow positions against gravity. The cell bodies of the trigeminal proprioceptive neurons in the mesencephalon potentially make gap-junctional connections with the locus coeruleus neurons. The locus coeruleus is implicated in arousal and autonomic function. Due to the relationship between arousal, ventromedial prefrontal cortex, and skin conductance, we assessed whether upgaze with trigeminal proprioceptive evocation activates sympathetically innervated sweat glands and the ventromedial prefrontal cortex. Specifically, we examined whether 60° upgaze induces palmar sweating and hemodynamic changes in the prefrontal cortex in 16 subjects. Sweating was monitored using a thumb-mounted perspiration meter, and prefrontal cortex activity was measured with 45-channel, functional near-infrared spectroscopy (fNIRS) and 2-channel NIRS at Fp1 and Fp2. In 16 subjects, palmar sweating was induced by upgaze and decreased in response to downgaze. Upgaze activated the ventromedial prefrontal cortex with an accumulation of integrated concentration changes in deoxyhemoglobin, oxyhemoglobin, and total hemoglobin levels in 12 subjects. Upgaze phasically and degree-dependently increased deoxyhemoglobin level at Fp1 and Fp2, whereas downgaze phasically decreased it in 16 subjects. Unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle used to significantly reduce trigeminal proprioceptive evocation ipsilaterally impaired the increased deoxyhemoglobin level by 60° upgaze at Fp1 or Fp2 in 6 subjects. We concluded that upgaze with strong trigeminal proprioceptive evocation was sufficient to phasically activate sympathetically innervated sweat glands and appeared to induce rapid oxygen consumption in the ventromedial prefrontal cortex and to rapidly produce deoxyhemoglobin to regulate physiological arousal. Thus, eyelid opening with trigeminal proprioceptive evocation may activate the ventromedial prefrontal cortex via the mesencephalic trigeminal nucleus and locus coeruleus.

No MeSH data available.


Related in: MedlinePlus

Palmar sweating response during a 60° upgaze for 5 s.(A–C) Three representative results showing various palmar sweating patterns. (D) No palmar sweating response in the same subject (C) on another day when he had insufficient sleep time. (E) The integrated absolute amounts of water loss during 5-s of 60° upgazes were compared with those in the preceding 5-s of 45° downgaze (*P < 0.05).
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pone.0134659.g002: Palmar sweating response during a 60° upgaze for 5 s.(A–C) Three representative results showing various palmar sweating patterns. (D) No palmar sweating response in the same subject (C) on another day when he had insufficient sleep time. (E) The integrated absolute amounts of water loss during 5-s of 60° upgazes were compared with those in the preceding 5-s of 45° downgaze (*P < 0.05).

Mentions: Palmar sweating responses commenced 1 to 6 s after initiating a 60° upgaze and increased rapidly without a plateau in 12 of 16 subjects (Fig 2A–2C). It decreased 1 to 9 s after beginning downgaze and persisted over a period of approximately 40 to 110 s. Increases in palmar sweating responses were not measured in 4 of 16 subjects who had insufficient sleep time. In the subjects with positive palmar sweating responses, 60° upgaze for 5 s did not induce sweating responses on another day when they had insufficient sleep time (Fig 2D). The median integrated absolute amount of water loss during 60° upgaze for 5 s (12.92 mg/cm2/min) was significantly larger (P < 0.05) than that for 5 s before 60° upgaze (10.79 mg/cm2/min) (Fig 2E).


Eyelid Opening with Trigeminal Proprioceptive Activation Regulates a Brainstem Arousal Mechanism.

Matsuo K, Ban R, Hama Y, Yuzuriha S - PLoS ONE (2015)

Palmar sweating response during a 60° upgaze for 5 s.(A–C) Three representative results showing various palmar sweating patterns. (D) No palmar sweating response in the same subject (C) on another day when he had insufficient sleep time. (E) The integrated absolute amounts of water loss during 5-s of 60° upgazes were compared with those in the preceding 5-s of 45° downgaze (*P < 0.05).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4526522&req=5

pone.0134659.g002: Palmar sweating response during a 60° upgaze for 5 s.(A–C) Three representative results showing various palmar sweating patterns. (D) No palmar sweating response in the same subject (C) on another day when he had insufficient sleep time. (E) The integrated absolute amounts of water loss during 5-s of 60° upgazes were compared with those in the preceding 5-s of 45° downgaze (*P < 0.05).
Mentions: Palmar sweating responses commenced 1 to 6 s after initiating a 60° upgaze and increased rapidly without a plateau in 12 of 16 subjects (Fig 2A–2C). It decreased 1 to 9 s after beginning downgaze and persisted over a period of approximately 40 to 110 s. Increases in palmar sweating responses were not measured in 4 of 16 subjects who had insufficient sleep time. In the subjects with positive palmar sweating responses, 60° upgaze for 5 s did not induce sweating responses on another day when they had insufficient sleep time (Fig 2D). The median integrated absolute amount of water loss during 60° upgaze for 5 s (12.92 mg/cm2/min) was significantly larger (P < 0.05) than that for 5 s before 60° upgaze (10.79 mg/cm2/min) (Fig 2E).

Bottom Line: Upgaze phasically and degree-dependently increased deoxyhemoglobin level at Fp1 and Fp2, whereas downgaze phasically decreased it in 16 subjects.Unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle used to significantly reduce trigeminal proprioceptive evocation ipsilaterally impaired the increased deoxyhemoglobin level by 60° upgaze at Fp1 or Fp2 in 6 subjects.We concluded that upgaze with strong trigeminal proprioceptive evocation was sufficient to phasically activate sympathetically innervated sweat glands and appeared to induce rapid oxygen consumption in the ventromedial prefrontal cortex and to rapidly produce deoxyhemoglobin to regulate physiological arousal.

View Article: PubMed Central - PubMed

Affiliation: Department of Plastic and Reconstructive Surgery, Shinshu University School of Medicine, Matsumoto, Japan.

ABSTRACT
Eyelid opening stretches mechanoreceptors in the supratarsal Müller muscle to activate the proprioceptive fiber supplied by the trigeminal mesencephalic nucleus. This proprioception induces reflex contractions of the slow-twitch fibers in the levator palpebrae superioris and frontalis muscles to sustain eyelid and eyebrow positions against gravity. The cell bodies of the trigeminal proprioceptive neurons in the mesencephalon potentially make gap-junctional connections with the locus coeruleus neurons. The locus coeruleus is implicated in arousal and autonomic function. Due to the relationship between arousal, ventromedial prefrontal cortex, and skin conductance, we assessed whether upgaze with trigeminal proprioceptive evocation activates sympathetically innervated sweat glands and the ventromedial prefrontal cortex. Specifically, we examined whether 60° upgaze induces palmar sweating and hemodynamic changes in the prefrontal cortex in 16 subjects. Sweating was monitored using a thumb-mounted perspiration meter, and prefrontal cortex activity was measured with 45-channel, functional near-infrared spectroscopy (fNIRS) and 2-channel NIRS at Fp1 and Fp2. In 16 subjects, palmar sweating was induced by upgaze and decreased in response to downgaze. Upgaze activated the ventromedial prefrontal cortex with an accumulation of integrated concentration changes in deoxyhemoglobin, oxyhemoglobin, and total hemoglobin levels in 12 subjects. Upgaze phasically and degree-dependently increased deoxyhemoglobin level at Fp1 and Fp2, whereas downgaze phasically decreased it in 16 subjects. Unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle used to significantly reduce trigeminal proprioceptive evocation ipsilaterally impaired the increased deoxyhemoglobin level by 60° upgaze at Fp1 or Fp2 in 6 subjects. We concluded that upgaze with strong trigeminal proprioceptive evocation was sufficient to phasically activate sympathetically innervated sweat glands and appeared to induce rapid oxygen consumption in the ventromedial prefrontal cortex and to rapidly produce deoxyhemoglobin to regulate physiological arousal. Thus, eyelid opening with trigeminal proprioceptive evocation may activate the ventromedial prefrontal cortex via the mesencephalic trigeminal nucleus and locus coeruleus.

No MeSH data available.


Related in: MedlinePlus