Limits...
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

Impaired activation of the ipsilateral ventromedial prefrontal cortex by unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle.Relative changes in the deoxyhemoglobin, oxyhemoglobin, total hemoglobin concentrations (mmol/L × cm) were measured at Fp1 and Fp2 according to the changes in the degree of eyelid retraction such as 45° downgaze (-45°), primary gaze (0°), 30° upgaze (+30°), and 60° upgaze (+60°) before (A1, B1, and C1) and after (A2, B2, and C2) anesthetization. Before anesthetization, three representative examples show bilateral activation (A1), asymmetrical bilateral activation (B1), and unilateral activation and contralateral deactivation for 5 s of 60° upgaze (+60°) (C1). After anesthetization, all of the examples show impaired activation at Fp1 or Fp2 on the anesthetized side (A2, B2, and C2). (D) On the anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was significantly smaller than that before anesthetization (*P < 0.01). However, on the non-anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was not significantly smaller than that before anesthetization.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4526522&req=5

pone.0134659.g006: Impaired activation of the ipsilateral ventromedial prefrontal cortex by unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle.Relative changes in the deoxyhemoglobin, oxyhemoglobin, total hemoglobin concentrations (mmol/L × cm) were measured at Fp1 and Fp2 according to the changes in the degree of eyelid retraction such as 45° downgaze (-45°), primary gaze (0°), 30° upgaze (+30°), and 60° upgaze (+60°) before (A1, B1, and C1) and after (A2, B2, and C2) anesthetization. Before anesthetization, three representative examples show bilateral activation (A1), asymmetrical bilateral activation (B1), and unilateral activation and contralateral deactivation for 5 s of 60° upgaze (+60°) (C1). After anesthetization, all of the examples show impaired activation at Fp1 or Fp2 on the anesthetized side (A2, B2, and C2). (D) On the anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was significantly smaller than that before anesthetization (*P < 0.01). However, on the non-anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was not significantly smaller than that before anesthetization.

Mentions: On the anesthetized side of more activated ventromedial prefrontal cortex by upgazes, the mean increase in the integrated deoxyhemoglobin values between 60° upgaze for 5 s and 45° downgaze for 5 s prior to the primary gaze (0°) after ipsilateral anesthetization (1.626 ± 1.298 mmol/L × cm) was significantly smaller than that before anesthetization (3.7554 ± 1.606 mmol/L × cm) (P<0.01) (Fig 6D). Conversely, on the non-administered side of less activated ventromedial prefrontal cortex by upgazes, although one subject showed degree-dependent decreases in deoxyhemoglobin concentrations by upgazes (Fig 6C1 and 6C2), the mean increase in the integrated deoxyhemoglobin values between 60° upgaze for 5 s and 45° downgaze for 5 s prior to the primary gaze (0°) after contralateral anesthetization (2.454 ± 2.852) was not significantly smaller than that before contralateral anesthetization (1.248 ± 2.328) (Fig 6D). Before anesthetization, tonic degree-dependent increases in deoxyhemoglobin concentrations were sustained compared to those during downgaze before 30°or 60° upgazing (Fig 6B1 and 6C1). However, after anesthetization, they were not sustained (Fig 6B2 and 6C2).


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

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

Impaired activation of the ipsilateral ventromedial prefrontal cortex by unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle.Relative changes in the deoxyhemoglobin, oxyhemoglobin, total hemoglobin concentrations (mmol/L × cm) were measured at Fp1 and Fp2 according to the changes in the degree of eyelid retraction such as 45° downgaze (-45°), primary gaze (0°), 30° upgaze (+30°), and 60° upgaze (+60°) before (A1, B1, and C1) and after (A2, B2, and C2) anesthetization. Before anesthetization, three representative examples show bilateral activation (A1), asymmetrical bilateral activation (B1), and unilateral activation and contralateral deactivation for 5 s of 60° upgaze (+60°) (C1). After anesthetization, all of the examples show impaired activation at Fp1 or Fp2 on the anesthetized side (A2, B2, and C2). (D) On the anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was significantly smaller than that before anesthetization (*P < 0.01). However, on the non-anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was not significantly smaller than that before anesthetization.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0134659.g006: Impaired activation of the ipsilateral ventromedial prefrontal cortex by unilateral anesthetization of mechanoreceptors in the supratarsal Müller muscle.Relative changes in the deoxyhemoglobin, oxyhemoglobin, total hemoglobin concentrations (mmol/L × cm) were measured at Fp1 and Fp2 according to the changes in the degree of eyelid retraction such as 45° downgaze (-45°), primary gaze (0°), 30° upgaze (+30°), and 60° upgaze (+60°) before (A1, B1, and C1) and after (A2, B2, and C2) anesthetization. Before anesthetization, three representative examples show bilateral activation (A1), asymmetrical bilateral activation (B1), and unilateral activation and contralateral deactivation for 5 s of 60° upgaze (+60°) (C1). After anesthetization, all of the examples show impaired activation at Fp1 or Fp2 on the anesthetized side (A2, B2, and C2). (D) On the anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was significantly smaller than that before anesthetization (*P < 0.01). However, on the non-anesthetized side, the increased integrated concentration of deoxyhemoglobin by 60° upgaze for 5 s after anesthetization was not significantly smaller than that before anesthetization.
Mentions: On the anesthetized side of more activated ventromedial prefrontal cortex by upgazes, the mean increase in the integrated deoxyhemoglobin values between 60° upgaze for 5 s and 45° downgaze for 5 s prior to the primary gaze (0°) after ipsilateral anesthetization (1.626 ± 1.298 mmol/L × cm) was significantly smaller than that before anesthetization (3.7554 ± 1.606 mmol/L × cm) (P<0.01) (Fig 6D). Conversely, on the non-administered side of less activated ventromedial prefrontal cortex by upgazes, although one subject showed degree-dependent decreases in deoxyhemoglobin concentrations by upgazes (Fig 6C1 and 6C2), the mean increase in the integrated deoxyhemoglobin values between 60° upgaze for 5 s and 45° downgaze for 5 s prior to the primary gaze (0°) after contralateral anesthetization (2.454 ± 2.852) was not significantly smaller than that before contralateral anesthetization (1.248 ± 2.328) (Fig 6D). Before anesthetization, tonic degree-dependent increases in deoxyhemoglobin concentrations were sustained compared to those during downgaze before 30°or 60° upgazing (Fig 6B1 and 6C1). However, after anesthetization, they were not sustained (Fig 6B2 and 6C2).

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