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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

Neuroanatomy of upgaze with trigeminal proprioceptive activation to regulate a brainstem arousal mechanism.Black arrows indicate voluntary contractions of the superior rectus and levator palpebrae superioris (LPSM) fast-twitch fibers via the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) and the oculomotor neurons. A red arrow indicates involuntary reflex contractions of the LPSM slow-twitch fibers. Green arrows indicate trigeminal proprioceptive stimulations to induce reflex contractions of the LPSM slow-twitch muscle fibers and stimulate the locus coeruleus (LC) via the mesencephalic trigeminal nucleus (MesV) through gap junctions. Blue arrows indicate efferent stimulations from the locus coeruleus (LC) to activate the ventromedial prefrontal cortex (vmPFC), palmar sweat glands, amygdala, and hippocampus. A blue dotted arrow indicates stimulation from the LC to the oculomotor neurons. The gray arrow indicates an afferent stimulation from the rostral ventrolateral medulla (RVLM) to the LC.
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pone.0134659.g001: Neuroanatomy of upgaze with trigeminal proprioceptive activation to regulate a brainstem arousal mechanism.Black arrows indicate voluntary contractions of the superior rectus and levator palpebrae superioris (LPSM) fast-twitch fibers via the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) and the oculomotor neurons. A red arrow indicates involuntary reflex contractions of the LPSM slow-twitch fibers. Green arrows indicate trigeminal proprioceptive stimulations to induce reflex contractions of the LPSM slow-twitch muscle fibers and stimulate the locus coeruleus (LC) via the mesencephalic trigeminal nucleus (MesV) through gap junctions. Blue arrows indicate efferent stimulations from the locus coeruleus (LC) to activate the ventromedial prefrontal cortex (vmPFC), palmar sweat glands, amygdala, and hippocampus. A blue dotted arrow indicates stimulation from the LC to the oculomotor neurons. The gray arrow indicates an afferent stimulation from the rostral ventrolateral medulla (RVLM) to the LC.

Mentions: We previously reported temporary or permanent blepharoptosis and brow ptosis after Müller muscle resection, lacrimal gland tumor resection with the lacrimal nerve, anesthesia of the Müller muscle or branches of the lacrimal nerve, and blowout fracture due to external force to the eyelid and globe [1–4]. We also previously reported that intraoperative stretching of the Müller muscle electromyographically induces an involuntary reflex contraction of the ipsilateral levator palpebrae superioris muscle (LPSM) [5]. This contraction appeared to correspond with the periodontal jaw muscle reflex as a model of reflex contractions of the LPSM slow-twitch fibers based on extrinsic mechanoreceptor stretching. Voluntary contractions of the jaw-closing fast-twitch muscle fibers stretch the extrinsic periodontal mechanoreceptor to evoke trigeminal proprioception, which in turn continuously induces reflex contractions of the jaw-closing slow-twitch muscle fibers via the mesencephalic trigeminal nucleus [6–9]. Thus, we have been exploring the extrinsic mechanoreceptors in the Müller muscle that induce reflex contractions of slow-twitch fibers in the LPSM and frontalis muscle to tonically sustain eyelid and eyebrow positions against gravity as well as elastic resistance [10] and its related mesencephalic trigeminal proprioceptive nucleus. The supratarsal Müller muscle, which is located between the LPSM and tarsus under the levator aponeurosis (Fig 1), is innervated not only by sparse, unmyelinated sympathetic efferent fibers but also by abundant, myelinated trigeminal proprioceptive afferent fibers [1, 2, 11]. The trigeminal proprioceptive fibers innervate the intramuscular connective tissues, including the interstitial cells of Cajal [11], which are like a palisade among the smooth muscle fibers and converge as a transverse nerve that runs on the proximal Müller muscle to join the lacrimal branch of the ophthalmic trigeminal nerve in humans [1]. Because the trigeminal proprioceptive neurons are connected to each other with gap junctions [12], Fluorogold, which passes through gap junctions, was applied as a tracer to the proximal stump of the trigeminal proprioceptive nerve in rats [3]. Fluorogold densely labeled the cell bodies of the trigeminal proprioceptive neurons in the ipsilateral mesencephalic trigeminal nucleus and a part of the locus coeruleus but not in any other rat brain region, including the trigeminal ganglion.


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

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

Neuroanatomy of upgaze with trigeminal proprioceptive activation to regulate a brainstem arousal mechanism.Black arrows indicate voluntary contractions of the superior rectus and levator palpebrae superioris (LPSM) fast-twitch fibers via the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) and the oculomotor neurons. A red arrow indicates involuntary reflex contractions of the LPSM slow-twitch fibers. Green arrows indicate trigeminal proprioceptive stimulations to induce reflex contractions of the LPSM slow-twitch muscle fibers and stimulate the locus coeruleus (LC) via the mesencephalic trigeminal nucleus (MesV) through gap junctions. Blue arrows indicate efferent stimulations from the locus coeruleus (LC) to activate the ventromedial prefrontal cortex (vmPFC), palmar sweat glands, amygdala, and hippocampus. A blue dotted arrow indicates stimulation from the LC to the oculomotor neurons. The gray arrow indicates an afferent stimulation from the rostral ventrolateral medulla (RVLM) to the LC.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0134659.g001: Neuroanatomy of upgaze with trigeminal proprioceptive activation to regulate a brainstem arousal mechanism.Black arrows indicate voluntary contractions of the superior rectus and levator palpebrae superioris (LPSM) fast-twitch fibers via the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) and the oculomotor neurons. A red arrow indicates involuntary reflex contractions of the LPSM slow-twitch fibers. Green arrows indicate trigeminal proprioceptive stimulations to induce reflex contractions of the LPSM slow-twitch muscle fibers and stimulate the locus coeruleus (LC) via the mesencephalic trigeminal nucleus (MesV) through gap junctions. Blue arrows indicate efferent stimulations from the locus coeruleus (LC) to activate the ventromedial prefrontal cortex (vmPFC), palmar sweat glands, amygdala, and hippocampus. A blue dotted arrow indicates stimulation from the LC to the oculomotor neurons. The gray arrow indicates an afferent stimulation from the rostral ventrolateral medulla (RVLM) to the LC.
Mentions: We previously reported temporary or permanent blepharoptosis and brow ptosis after Müller muscle resection, lacrimal gland tumor resection with the lacrimal nerve, anesthesia of the Müller muscle or branches of the lacrimal nerve, and blowout fracture due to external force to the eyelid and globe [1–4]. We also previously reported that intraoperative stretching of the Müller muscle electromyographically induces an involuntary reflex contraction of the ipsilateral levator palpebrae superioris muscle (LPSM) [5]. This contraction appeared to correspond with the periodontal jaw muscle reflex as a model of reflex contractions of the LPSM slow-twitch fibers based on extrinsic mechanoreceptor stretching. Voluntary contractions of the jaw-closing fast-twitch muscle fibers stretch the extrinsic periodontal mechanoreceptor to evoke trigeminal proprioception, which in turn continuously induces reflex contractions of the jaw-closing slow-twitch muscle fibers via the mesencephalic trigeminal nucleus [6–9]. Thus, we have been exploring the extrinsic mechanoreceptors in the Müller muscle that induce reflex contractions of slow-twitch fibers in the LPSM and frontalis muscle to tonically sustain eyelid and eyebrow positions against gravity as well as elastic resistance [10] and its related mesencephalic trigeminal proprioceptive nucleus. The supratarsal Müller muscle, which is located between the LPSM and tarsus under the levator aponeurosis (Fig 1), is innervated not only by sparse, unmyelinated sympathetic efferent fibers but also by abundant, myelinated trigeminal proprioceptive afferent fibers [1, 2, 11]. The trigeminal proprioceptive fibers innervate the intramuscular connective tissues, including the interstitial cells of Cajal [11], which are like a palisade among the smooth muscle fibers and converge as a transverse nerve that runs on the proximal Müller muscle to join the lacrimal branch of the ophthalmic trigeminal nerve in humans [1]. Because the trigeminal proprioceptive neurons are connected to each other with gap junctions [12], Fluorogold, which passes through gap junctions, was applied as a tracer to the proximal stump of the trigeminal proprioceptive nerve in rats [3]. Fluorogold densely labeled the cell bodies of the trigeminal proprioceptive neurons in the ipsilateral mesencephalic trigeminal nucleus and a part of the locus coeruleus but not in any other rat brain region, including the trigeminal ganglion.

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