Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
feipeng wu
 + 2906 word(s) 2906 2022-01-14 10:27:48 |
2 format corrected.
Beatrix Zheng
 + 62 word(s) 2968 2022-01-19 09:00:44 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Wu, F. Ocular Autonomic Nervous System. Encyclopedia. Available online: https://encyclopedia.pub/entry/18473 (accessed on 17 May 2024).
Wu F. Ocular Autonomic Nervous System. Encyclopedia. Available at: https://encyclopedia.pub/entry/18473. Accessed May 17, 2024.
Wu, Feipeng. "Ocular Autonomic Nervous System" Encyclopedia, https://encyclopedia.pub/entry/18473 (accessed May 17, 2024).
Wu, F. (2022, January 19). Ocular Autonomic Nervous System. In Encyclopedia. https://encyclopedia.pub/entry/18473
Wu, Feipeng. "Ocular Autonomic Nervous System." Encyclopedia. Web. 19 January, 2022.
Ocular Autonomic Nervous System
Edit
This entry is adapted from the peer-reviewed paper 10.3390/vision6010006

The autonomic nervous system (ANS) confers neural control of the entire body, mainly through the sympathetic and parasympathetic nerves. Several studies have observed that the physiological functions of the eye (pupil size, lens accommodation, ocular circulation, and intraocular pressure regulation) are precisely regulated by the ANS. Almost all parts of the eye have autonomic innervation for the regulation of local homeostasis through synergy and antagonism. With the advent of new research methods, novel anatomical characteristics and numerous physiological processes have been elucidated.

autonomic nervous system eye anatomy pupil light reflex choroidal blood flow aqueous humor

1. Autonomic Control of the Eye

1.1. Cornea

The cornea is one of the most densely innervated parts of the human body with a rich supply of sensory and autonomic nerve fibers [1]. Sensory nerves, mainly originating from the ophthalmic branch of the trigeminal nerve, comprise the majority of the nerves in the cornea. Sympathetic nerves originating from the SCG are found in the corneas of mammals, and their densities vary in different species. Parasympathetic innervation originating from the CG has been also reported in cats and rats [2][3][4].
The corneal innervation was first described in detail in 1951 [5], but the description of human corneal nerves was relatively limited at that time. Recent studies have suggested that nerve bundles enter the peripheral cornea radially and parallel to the corneal surface; thereupon, they lose their perineurium and myelin sheaths at approximately 1 mm from the limbus and about 0.1 nm from the ocular surface. These nerve bundles radiate through the middle third of the corneal stroma and further subdivide to form smaller branches that comprise a moderately dense midstromal plexus and a dense subepithelial plexus (SEP) before finally passing through the anterior elastic layer and entering the corneal epithelium [3][6][7].
These sensory and autonomic nerves also play a key role in maintaining the optimal health of the ocular surface. Corneal nerves can release soluble trophic substances that promote lacrimal gland secretion, induce blinking reflexes, and maintain the integrity of the ocular surface [8]. Substance P (SP) exerts a strong synergistic effect with insulin-like growth factor-1 (IGF-1) or epidermal growth factor to promote corneal epithelial migration, adhesion, and wound closure. Several other neuropeptides also play important roles in the cornea (Table 1) [9][10][11].
Table 1. Various peptide and transmitters in the cornea of mammals.
Compound. Mechanism
Substance P Epithelial renewal and wound repair
CGRP Epithelial renewal and wound repair
Norepinephrine Epithelial renewal and wound repair; stimulate proliferation and migration of corneal epithelial cells
Acetylcholine Promote DNA synthesis in epithelial cells
VIP Protect corneal endothelial cells from oxidative stress
Neurotensin Increases keratocyte proliferation; decreases keratocycte apoptosis
Nerve growth factor Sustain homeostasis and regeneration of epithelium and stroma

1.2. Iris

The iris is a circular pigmented membrane located in front of the lens, it divides the cavity between the cornea and lens into an anterior chamber and a posterior chamber.
The iris controls the amount of light entering the eye by adjusting the pupil. The preganglionic parasympathetic axons originating from the EWpg innervate the pupillary sphincter through the short ciliary nerve. These axons act on the muscarinic receptors of the pupillary sphincter, and mediate pupillary constriction. Sympathetic innervation originates from the SCG and provides a reciprocal function via the long ciliary nerves which control pupil dilation [12][13]. The ophthalmic nerve, a branch of the trigeminal nerve, is also involved in the innervation of the iris [14]. Previous studies have suggested that the trigeminal nerve offers sensory transduction and induces substance P-related contractions for mediating protective reflexes [15]. However, recent studies have demonstrated that the trigeminal nerve also affects smooth muscle response, intraocular blood vessels, and immune function by releasing various peptides [12]. Based on these anatomical functions and innervations, pupil evaluation can be a simple and convenient method to detect autonomic disorders and may therefore have potential diagnostic value [16].
The iris of several vertebrate species has rhodopsin, a molecule that enables photomechanical responses (PMR). Rhodopsin enables pupillary constriction in response to light without the need for a central nervous reflex. This process may involve (1) rhodopsin-activated G-protein, (2) phospholipase C, (3) inositol triphosphate, or (4) Ca2+ [17][18]. Moreover, PMR can be inhibited by β-adrenergic agonists, but not by α-adrenergic agonists [18][19]. After the application of β-adrenergic agonist to toad sphincter cells, the availability of Ca2+ ions for sphincter contraction was found to be altered, followed by pupillary dilation [19]. Generally, the sympathetic and parasympathetic systems work antagonistically to control the contraction and relaxation of the iris muscles. The ratio of innervations from these systems differs among species [12].

1.3. Anterior Chamber Angle

The main outflow pathway of aqueous humor (AH) comprises the trabecular meshwork (TM), the endothelial lining of Schlemm’s canal, juxtacanalicular connective tissue, collecting channels, and aqueous veins. Additionally, the outflow resistance of the TM pathway seems to be regulated by the contraction of the scleral spur (SS) cells and ciliary muscles [20]. In almost all species, the SS cells contain SP-positive axons, most of which also immunostain for CGRP [14][21]. In humans, the axons in the TM and SS show immunoreactivity (IR) to SP, CGRP, NPY, VIP, and NOS, while in monkeys, sympathetic SS cell innervations are more frequently observed [22][23][24][25][26]. These cholinergic and nitrergic nerve terminals may induce the contraction and relaxation of TM and SS cells [27]. However, research on human and monkey eyes has shown few TH-positive and VIP-positive nerve fibers, as well as the absence of NPY-positive fibers in SS and TM [27]. Only a small amount of opioid peptidergic innervation has been reported in the anterior eye segment of the eye in rats. SP, CGRP, NPY, and VIP immunoreactivity also occurs in the ciliary process, ciliary muscles, and ciliary blood vessels [28]. A recent study demonstrated the presence of efferent nerve pathways from the hypothalamus to the autonomic innervation in the bilateral anterior chamber [29]. When inflammation occurs, peptide expression in the bilateral anterior chamber is upregulated [30]. The immunolabeling pattern for TM is similar in humans and pigs [31].
Nomura found that approximately one-third of the innervation in the TM is sympathetic in monkeys, and that two-thirds are parasympathetic [32]. In human TM and cultured TM cells, most receptors on the sympathetic nerves appear to be the β2 adrenergic subtype [33][34].

1.4. Lacrimal Glands

The lacrimal gland is located in the orbit of the human eye. Lacrimal secretions are vital to the health and maintenance of the cells on the ocular surface (conjunctiva, corneal epithelium). Regulation of lacrimal gland secretion involves the following: (1) stimulation of the sensory nerve on the ocular surface and (2) parasympathetic and sympathetic activation of the lacrimal secretory cells [35]. Mechanonociceptors, polymodal nociceptors, and cold receptor fibers are distributed on the conjunctiva and cornea [36][37]. Stimulation of the corneal polymodal nociceptors causes reflex tear secretion, while mechanonociceptors and cold receptors are less effective in mediating this effect. Interestingly, tear secretion does not increase with increased stimulation of the conjunctival receptors [38].
Tear production is regulated by both the sympathetic and parasympathetic nerves. Generally, sympathetic nerves affect tear secretion via the following two methods: (1) alteration of blood flow [39] and (2) via increased secretion of sympathetic neurotransmitters [40][41]. However, the role of sympathetic nerves in the lacrimal gland remains uncertain. Some studies have suggested that electrostimulation of the SCG alters tear secretion, while other studies report contradictory findings [42][43][44]. The content of the tear secretion remains unaltered even after SCG ablation, indicating that tear secretion is not related to sympathetic postganglionic nerves [45]. Tear secretion is mainly controlled by the parasympathetic nerves [45]. These nerves mediate tear secretion by releasing Ach and activating the M3 muscarinic Ach receptors [46][47]. Moreover, marked reduction in lacrimal gland secretion can be observed in rabbits with parasympathetic nerve lesions [48].

1.5. Retina

The neural retina is a layered structure that converts photic illumination into visual information and then transmits this signal to the brain. The retinal circulation and the choroidal circulation, both of which originate from the ophthalmic artery, are responsible for supplying oxygen and nutrition to the retina. Retinal circulation provides a low level of blood flow and a high level of oxygen extraction, contrary to that in choroidal circulation [49][50]. There is limited insufficient evidence of autonomic innervation in the intraocular branch of the central retinal artery (CRA) [51][52]. Instead, retinal circulation is generally considered to be autoregulated by local mechanical and chemical stimulations based on the sensation of the oxygen levels [53][54].
The preocular CRA in humans receives adrenergic and cholinergic nerve fibers, suggesting sympathetic and parasympathetic innervation. However, SP, CGRP, and VIP were not detected in the nerve fibers, indicating a lack of peptidergic innervation [55]. Similarly, immunohistochemical and histochemical studies have confirmed the presence of [48] parasympathetic nerve (NOS/VIP/NADPH-d), sympathetic nerve (TH), and CGRP-positive afferent nerve fibers in the vicinity of the monkey and rat CRA [56][57]. Substance P-positive nerve fibers have also been identified around the CRA in rabbits [58]. Early research on several monkey species has shown that adrenergic innervation is only present posterior to the lamina cribosa in the intraorbital part of the optic nerve [52][59]. Postganglionic nerves of the pterygopalatine ganglion release NO, causing vasodilation of the arterial smooth muscles [60][61]. The sympathetic innervation gradually decreases with increasing age [62], which may lead to significant loss of photoreceptor cells and increased reactivity of the glial cells [63].

1.6. Choroid

The choroid makes up the posterior part of the uvea, located between the retina and sclera, and is mainly composed of blood vessels. Neurons in the choroid, which mainly regulate choroidal circulation, are also called choroidal ganglion cells or intrinsic choroidal neurons (ICN) [64][65]. There are approximately 2000 ICNs in each eye. Most of these ICNs are clustered in the temporal and central regions of the submacular area. In contrast, these neurons are largely accumulated at the periphery in rabbits, possibly because rabbits lack the macula [66]. In other species, there are only approximately 500 ICNs, with largely uniform distribution. In different avian species, the number of ICNs varies from less than 500 in quail to more than 6000 in geese. These cells are mainly concentrated at the temporocranial area in Galliformes, while in Anseriformes, they form a belt that extends in the cranionasal to temporocaudal direction [67].
In mammals, the primary input of the parasympathetic nerves originates from the PPG via the facial nerve [68][69]. Although some physiological changes have been noted upon stimulation of the CG, the innervation of the choroid in mammals has not been confirmed to date [70][71][72]. However, in avian, the CG supplies most of the parasympathetic innervation [73], these parasympathetic input increases choroidal blood flow of via vasodilation. On immunohistochemistry, almost all ICGs are stained for nNOS and VIP, half of the cells show immunoreactivity for calretinin, while the individual cells are stained only for just neuropeptide Y (NPY) [74][64]. The choroid contains large amounts of TH(+) and NPY(+) ICNs in the central temporal area [75]. Using immunohistochemistry method, sympathetic innervation was observed derived from the SCG and modulates the NO/VIP/GAL innervation of vascular and non-vascular smooth muscle provided by ICN [76][77]. Such dual innervation balances the increase and decrease in choroid blood flow. Despite aging, the choroidal innervation patterns and neural transmitters remain unaltered to some extent [64]; however, some studies have suggested a decrease in adrenergic fibers and VIP(+) nerve fibers [78][79][80]. SP (+) and CGRP (+) ICNs have been identified in choroidal whole mounts, suggesting choroidal innervation by sensory nerves. Additionally, these ICNs were found to be more concentrated in the temporal and central regions and are thought to be involved in mediating blood flow and vascular architecture [81].

2. Physiological Effect

2.1. Pupil Adjustment

The size of the pupil varies with the intensity of incident ambient light, which forms the PLR. Generally, pupil dilation and constriction depends on both autonomic innervation and local reflexes [82]. Light incident into one eye can cause constriction of both the eyes, including the unstimulated eye. These phenomena are termed direct and consensual responses. In early studies, the consensual response was thought to be limited to “higher” mammals. However, recent studies have provided more evidence to support that consensual response also occurs in “lower” mammals, and even non-mammals; although, in non-mammalian species, consensual PLR is indistinctive [83][84].

2.2. Ocular Blood Flow

There are no blood vessels in the normal cornea, while the limbus contains abundant blood vessels that supply nutrients and oxygen. Similar to the cornea, the scleral stromal layer has no blood vessels, except those passing through. However, the sclera surface and optic nerve lamina cribrosa are rich in blood vessels and form a vascular network. These arteries are derived from the ophthalmic artery, which is the only artery supplying the eye. This blood vessel receives autonomic innervation and mainly supplies the uvea and retina. Hence, nearly all ocular circulation is modulated by autonomic nerves, except the retinal blood vessels [53].
The choroidal circulatory system is responsible for supplying the photoreceptors and the retinal pigment epithelium. Reduced blood flow can cause a rapid loss of photoreceptor cells [85]. Generally, autonomic innervation of the choroid includes parasympathetic pathways that dilate vessels and increase blood flow, sympathetic pathways that constrict vessels and decrease blood flow, and the local trigeminal system that transfers sensory input, or directly releases SP/CGRP in response to activating stimuli [86].
The SSN–PPG circuit mediates choroidal parasympathetic vasodilation, which seems to contribute to ChBF pressure regulation in case of low arterial blood pressure (ABP) [87][68]. In mammals, the PPG receives parasympathetic input from the SSN [88], and its preganglionic root, which contains NOS, VIP, and ChAT, directly projects to the choroid [89]. Many studies have discussed the role of VIP, NO, and ACh in mediating ChBF after stimulation of the facial nerve or SSN. Intravenous injection of VIP leads to increased intraocular pressure (IOP) and ChBF [90]. Different vasoactive substances affect the excitation frequencies of different nerves. In rabbits, the formation of NO (endothelial or neurogenic) is involved in uveal vasodilation caused by low-frequency facial nerve stimulation, while at high frequencies, other neurotransmitters also seem to be involved [91]. ChBF was significantly increased following facial nerve stimulation in monkeys, cats, and rabbits. Moreover, VIP was suggested as the peripheral molecule causing the vasodilation [92].
Based on immunohistochemical experiments in pigeons, the PPG seem to be composed of three to four main sub-ganglia connected to each other. Each main nerve contains 50–200 neurons, as well as several small ganglia. These neurons in birds release VIP and NO, and possibly Ach [93]. In mammals, the regulatory effect of PPG on ChBF appears to be similar as that in birds and can partially compensate for the decreased ABP. This may be a common ocular mechanism in warm-blooded vertebrates [94]. The avian choroid has a distinctive parasympathetic input of the CG and occupies a dominant position [86]. Using anatomical knowledge and electrical stimulation experiments, the central components from circuits in avian ChBF regulation were identified as follows: the retina–contralateral SCN that contains SP (+) neurons–medial EW (EWm), which controls ChBF via its ipsilateral projection to choroidal neurons of the CG [95]. Cantwell and Cassone indicated that SCN in avians can be divided into medial SCN (mSCN) and visual SCN (vSCN), while the latter is considered to participate in ChBF regulation [96][97]. If SCN was activated by retinal illumination of the contralateral eye, the choroidal volume appeared to increase (vasodilation) corresponding to a similar increase in systemic blood pressure [98]. This complex parasympathetic reflex response might be adaptive and is involved in maintaining the health of photoreceptor cells [99]. Cholinergic fibers of the CG are widely distributed in the choroid of avians. M2, M3, and M4 type receptors have been found in the retina, retinal pigment epithelium, choroid, and ciliary body [100]. After specifically suppressing these muscarinic receptors, M3 muscarinic receptors were observed to dominantly facilitate the EW-mediated increase in ChBF, with endothelial cell stimulation to release NO [101].
In both mammals and birds, the sympathetic nerves innervating the choroid are derived from noradrenergic nerve fibers of the cervical ganglia [86]. Stimulating the unilateral sympathetic nerve causes a large reduction in the ChBF [102][103]. After ICN transection, the choroids demonstrate increased vascularity and sympathetic denervation of the choroid and retinal defects [104][105]. These effects may be mediated by adrenoceptors. Previous research suggested that α-and β-adrenergic blocks can cause choroidal vasodilation and vasoconstriction, respectively, in rabbits [106]. This result is consistent with the observation that venous NPY treatment significantly reduces ChBF [107]. The trigeminal nerve branches that contain SP and CGRP innervate the choroid in mammals and birds [28]. Trigeminal nerve stimulation leads to the local release of vasodilators, SP, and CGRP [108]. Some researchers have recognized that the TG may be involved in the temperature-dependent regulation of ChBF. However, the specific underlying mechanisms need to be further investigated [86].

2.3. Intraocular Pressure Regulation

Aqueous humor (AH) is a transparent fluid found in the anterior and posterior chambers. It is mainly responsible for nutrient delivery and IOP regulation. It is produced by the ciliary epithelium and exits the eye through two independent outflow pathways, which involves the trabecular meshwork (TM) and unconventional pathway (uveoscleral). Recent evidence has suggested that another unconventional pathway (uveolymphatic route) has potential for maintaining IOP [109].

2.4. Lens Accommodation

The accommodation reflex, also referred as near reflex, is the response for focusing on near objects [110]. The afferent limb of this reflex is through the optic nerve and efferent limb was considered to be the EWpg, EWcp, and the oculomotor [111]. The final effects of this reflex consists the convergence of both eyes and contraction of the ciliary muscle leading to the change of lens accommodation and pupillary constriction [112]. The ciliary muscle of mammals, and its homologues in fish and amphibia are contracted via cholinergic muscarinic mechanisms, while in birds and reptiles, acetylcholine acts via nicotinic receptors [12].
Recent research on primates suggested that the premotor neurons controlling the lens of unilateral eye are distributed in the bilateral midbrain. By retrograde tracing methods, some of the premotor neurons in the supraoculomotor area and central mesencephalic formation were doubly labeled, while others were labeled from either the ipsilateral or contralateral eye, which suggest the both monocular control and binocular control of lens accommodation [113].
Because of all the recent and past work that has been performed, lens accommodation to vergence angle and other aspects of eye movements are connected [113][114][115][116]. A cohort study showed that with lens accommodation, anterior chamber depth, and anterior chamber angle remained stable while the pupil diameter varied [117].

References

  1. Yang, A.Y.; Chow, J.; Liu, J. Corneal Innervation and Sensation: The Eye and Beyond. Yale J. Biol. Med. 2018, 91, 13–21.
  2. Marfurt, C.F.; Kingsley, R.E.; Echtenkamp, S.E. Sensory and sympathetic innervation of the mammalian cornea. A retrograde tracing study. Investig. Ophthalmol. Vis. Sci. 1989, 30, 461–472.
  3. Müller, L.J.; Marfurt, C.F.; Kruse, F.; Tervo, T.M. Corneal nerves: Structure, contents and function. Exp. Eye Res. 2003, 76, 521–542.
  4. Medeiros, C.S.; Santhiago, M.R. Corneal nerves anatomy, function, injury and regeneration. Exp. Eye Res. 2020, 200, 108243.
  5. Zander, E.; Weddell, G. Observations on the innervation of the cornea. J. Anat. 1951, 85, 68–99.
  6. Al-Aqaba, M.A.; Fares, U.; Suleman, H.; Lowe, J.; Dua, H.S. Architecture and distribution of human corneal nerves. Br. J. Ophthalmol. 2009, 94, 784–789.
  7. Müller, L.J.; Pels, L.; Vrensen, G.F. Ultrastructural organization of human corneal nerves. Investig. Ophthalmol. Vis. Sci. 1996, 37, 476–488.
  8. Stern, M.E.; Beuerman, R.W.; Fox, R.I.; Gao, J.; Mircheff, A.K.; Pflugfelder, S.C. The Pathology of Dry Eye. Cornea 1998, 17, 584–589.
  9. Ghiasi, Z.; Gray, T.; Tran, P.; Dubielzig, R.; Murphy, C.; McCartney, D.L.; Reid, T.W. The Effect of Topical Substance-P Plus Insulin-like Growth Factor-1 (IGF-1) on Epithelial Healing After Photorefractive Keratectomy in Rabbits. Transl. Vis. Sci. Technol. 2018, 7, 12.
  10. Suvas, S. Role of Substance P Neuropeptide in Inflammation, Wound Healing, and Tissue Homeostasis. J. Immunol. 2017, 199, 1543–1552.
  11. Nakamura, M.; Nishida, T.; Ofuji, K.; Reid, T.W.; Mannis, M.J.; Murphy, C.J. Synergistic Effect of Substance P with Epidermal Growth Factor on Epithelial Migration in Rabbit Cornea. Exp. Eye Res. 1997, 65, 321–329.
  12. Neuhuber, W.; Schrödl, F. Autonomic control of the eye and the iris. Auton. Neurosci. 2011, 165, 67–79.
  13. Kawasaki, A. Physiology, assessment, and disorders of the pupil. Curr. Opin. Ophthalmol. 1999, 10, 394–400.
  14. Stone, R.; Laties, A.; Brecha, N. Substance P-like immunoreactive nerves in the anterior segment of the rabbit, cat and monkey eye. Neuroscience 1982, 7, 2459–2468.
  15. Fujiwara, M.; Hayashi, H.; Muramatsu, I.; Ueda, N. Supersensitivity of the rabbit iris sphincter muscle induced by trigeminal denervation: The role of substance P. J. Physiol. 1984, 350, 583–597.
  16. Bremner, F. Pupil evaluation as a test for autonomic disorders. Clin. Auton. Res. 2009, 19, 88–101.
  17. Hardie, R.C.; Franze, K. Photomechanical Responses in Drosophila Photoreceptors. Science 2012, 338, 260–263.
  18. Barr, L. Photomechanical coupling in the vertebrate sphincter pupillae. Crit. Rev. Neurobiol. 1989, 4, 325–366.
  19. Rubin, L.J.; Nolte, J.F. Modulation of the response of a photosensitive muscle by β-adrenergic regulation of cyclic AMP levels. Nature 1984, 307, 551–553.
  20. Tamm, E.R. The trabecular meshwork outflow pathways: Structural and functional aspects. Exp. Eye Res. 2009, 88, 648–655.
  21. Ruskell, G.L. Trigeminal innervation of the scleral spur in cynomolgus monkeys. J. Anat. 1994, 184, 511–518.
  22. Tamm, E.R.; Koch, T.A.; Mayer, B.; Stefani, F.H.; Lütjen-Drecoll, E. Innervation of myofibroblast-like scleral spur cells in human monkey eyes. Investig. Ophthalmol. Vis. Sci. 1995, 36, 1633–1644.
  23. Stone, R.A. Neuropeptide Y and the innervation of the human eye. Exp. Eye Res. 1986, 42, 349–355.
  24. Stone, R.A.; Tervo, T.; Tervo, K.; Tarkkanen, A. Vasoactive intestinal polypeptide-like immunoreactive nerves to the human eye. Acta Ophthalmol. 1986, 64, 12–18.
  25. Laties, A.M.; Stone, R.A.; Brecha, N.C. Substance P-like immunoreactive nerve fibers in the trabecular meshwork. Investig. Ophthalmol. Vis. Sci. 1981, 21, 484–486.
  26. Stone, R.A.; McGlinn, A.M. Calcitonin gene-related peptide immunoreactive nerves in human and rhesus monkey eyes. Investig. Ophthalmol. Vis. Sci. 1988, 29, 305–310.
  27. Selbach, J.M.; Gottanka, J.; Wittmann, M.; Lütjen-Drecoll, E. Efferent and afferent innervation of primate trabecular meshwork and scleral spur. Investig. Ophthalmol. Vis. Sci. 2000, 41, 2184–2191.
  28. Stone, R.A.; Kuwayama, Y.; Laties, A.M. Regulatory peptides in the eye. Experientia 1987, 43, 791–800.
  29. Yang, F.; Zhu, X.; Liu, X.; Ma, L.; Zhang, Z.; Pei, L.; Wang, H.; Xu, F.; Liu, H. Anatomical evidence for the efferent pathway from the hypothalamus to autonomic innervation in the anterior chamber structures of eyes. Exp. Eye Res. 2020, 202, 108367.
  30. Selbach, J.M.; Buschnack, S.H.; Steuhl, K.-P.; Kremmer, S.; Muth-Selbach, U. Substance P and opioid peptidergic innervation of the anterior eye segment of the rat: An immunohistochemical study. J. Anat. 2005, 206, 237–242.
  31. May, C.A.; Skorski, L.M.; Lutjen-Drecoll, E. Innervation of the porcine ciliary muscle and outflow region. J. Anat. 2005, 206, 231–236.
  32. Nomura, T.; Smelser, G.K. The identification of adrenergic and cholinergic nerve endings in the trabecular meshwork. Investig. Ophthalmol. 1974, 13, 525–532.
  33. Jampel, H.D.; Lynch, M.G.; Brown, R.H.; Kuhar, M.J.; De Souza, E.B. Beta-adrenergic receptors in human trabecular meshwork. Identification and autoradiographic localization. Investig. Ophthalmol. Vis. Sci. 1987, 28, 772–779.
  34. Wax, M.B.; Molinoff, P.B.; Alvarado, J.; Polansky, J. Characterization of beta-adrenergic receptors in cultured human trabecular cells and in human trabecular meshwork. Investig. Ophthalmol. Vis. Sci. 1989, 30, 51–57.
  35. Dartt, D.A. Neural regulation of lacrimal gland secretory processes: Relevance in dry eye diseases. Prog. Retin. Eye Res. 2009, 28, 155–177.
  36. Acosta, M.C.; Belmonte, C.; Gallar, J. Sensory experiences in humans and single-unit activity in cats evoked by polymodal stimulation of the cornea. J. Physiol. 2001, 534, 511–525.
  37. Gallar, J.; Pozo, M.A.; Tuckett, R.P.; Belmonte, C. Response of sensory units with unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat’s cornea. J. Physiol. 1993, 468, 609–622.
  38. Acosta, M.C.; Peral, A.; Luna, C.; Pintor, J.; Belmonte, C.; Gallar, J. Tear Secretion Induced by Selective Stimulation of Corneal and Conjunctival Sensory Nerve Fibers. Investig. Opthalmol. Vis. Sci. 2004, 45, 2333–2336.
  39. Botelho, S.; Martinez, E.; Pholpramool, C.; Prooyen, H.; Janssen, J.; De Palau, A. Modification of stimulated lacrimal gland flow by sympathetic nerve impulses in rabbit. Am. J. Physiol. Content 1976, 230, 80–84.
  40. Adeghate, E.; Singh, J.; Howarth, F.C.; Burrows, S. Control of porcine lacrimal gland secretion by non-cholinergic, non-adrenergic nerves: Effects of electrical field stimulation, VIP and NPY. Brain Res. 1997, 758, 127–135.
  41. Ding, C.; Walcott, B.; Keyser, K.T. Sympathetic Neural Control of the Mouse Lacrimal Gland. Investig. Opthalmol. Vis. Sci. 2003, 44, 1513–1520.
  42. Meneray, M.A.; Bennett, D.J.; Nguyen, D.H.; Beuerman, R.W. Effect of Sensory Denervation on the Structure and Physiologic Responsiveness of Rabbit Lacrimal Gland. Cornea 1998, 17, 99–107.
  43. Ruskell, G.L. Changes in nerve terminals and acini of the lacrimal gland and changes in secretion induced by autonomic denervation. Z. Für Zellforsch. Und Mikrosk. Anat. 1969, 94, 261–281.
  44. Tangkrisanavinont, V. Stimulation of lacrimal secretion by sympathetic nerve impulses in the rabbit. Life Sci. 1984, 34, 2365–2371.
  45. Jin, K.; Imada, T.; Hisamura, R.; Ito, M.; Toriumi, H.; Tanaka, K.; Nakamura, S.; Tsubota, K. Identification of Lacrimal Gland Postganglionic Innervation and Its Regulation of Tear Secretion. Am. J. Pathol. 2020, 190, 1068–1079.
  46. Nakamura, M.; Tada, Y.; Akaishi, T.; Nakata, K. M3 muscarinic receptor mediates regulation of protein secretion in rabbit lacrimal gland. Curr. Eye Res. 1997, 16, 614–619.
  47. Mauduit, P.; Jammes, H.; Rossignol, B. M3 muscarinic acetylcholine receptor coupling to PLC in rat exorbital lacrimal acinar cells. Am. J. Physiol. Physiol. 1993, 264, C1550–C1560.
  48. Toshida, H.; Nguyen, A.H.; Beuerman, R.W.; Murakami, A. Evaluation of Novel Dry Eye Model: Preganglionic Parasympathetic Denervation in Rabbit. Investig. Opthalmol. Vis. Sci. 2007, 48, 4468–4475.
  49. Alm, A.; Bill, A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): A study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp. Eye Res. 1973, 15, 15–29.
  50. Törnquist, P.; Alm, A. Retinal and choroidal contribution to retinal metabolism in vivo. A study in pigs. Acta Physiol. Scand. 1979, 106, 351–357.
  51. Hogan, M.J.; Feeney, L. The ultrastructure of the retinal blood vessels: I. The large vessels. J. Ultrastruct. Res. 1963, 9, 10–28.
  52. Laties, A.M. Central Retinal Artery Innervation. Arch. Ophthalmol. 1967, 77, 405–409.
  53. Delaey, C.; Van De Voorde, J. Regulatory Mechanisms in the Retinal and Choroidal Circulation. Ophthalmic Res. 2000, 32, 249–256.
  54. Ferrari-DiLeo, G.; Davis, E.B.; Anderson, D.R. Biochemical evidence for cholinergic activity in retinal blood vessels. Investig. Ophthalmol. Vis. Sci. 1989, 30, 473–477.
  55. Bergua, A.; Kapsreiter, M.; Neuhuber, W.L.; Reitsamer, H.A.; Schrödl, F. Innervation pattern of the preocular human central retinal artery. Exp. Eye Res. 2013, 110, 142–147.
  56. Bergua, A.; Schrödl, F.; Neuhuber, W.L. Vasoactive intestinal and calcitonin gene-related peptides, tyrosine hydroxylase and nitrergic markers in the innervation of the rat central retinal artery. Exp. Eye Res. 2003, 77, 367–374.
  57. Ye, X.D.; Laties, A.M.; Stone, R.A. Peptidergic innervation of the retinal vasculature and optic nerve head. Investig. Ophthalmol. Vis. Sci. 1990, 31, 1731–1737.
  58. Kumagai, N.; Yuda, K.; Kadota, T.; Goris, R.C.; Kishida, R. Substance P-like immunoreactivity in the central retinal artery of the rabbit. Exp. Eye Res. 1988, 46, 591–596.
  59. Laties, A.M.; Jacobowitz, D. A comparative study of the autonomic innervation of the eye in monkey, cat, and rabbit. Anat. Rec. Adv. Integr. Anat. Evol. Biol. 1966, 156, 383–395.
  60. Toda, N.; Toda, M.; Ayajiki, K.; Okamura, T. Monkey central retinal artery is innervated by nitroxidergic vasodilator nerves. Investig. Ophthalmol. Vis. Sci. 1996, 37, 2177–2184.
  61. Toda, N.; Ayajiki, K.; Yoshida, K.; Kimura, H.; Okamura, T. Impairment by damage of the pterygopalatine ganglion of nitroxidergic vasodilator nerve function in canine cerebral and retinal arteries. Circ. Res. 1993, 72, 206–213.
  62. Smith, C.P.; Sharma, S.; Steinle, J. Age-related changes in sympathetic neurotransmission in rat retina and choroid. Exp. Eye Res. 2007, 84, 75–81.
  63. Steinle, J.J.; Lindsay, N.L.; Lashbrook, B.L. Cervical sympathectomy causes photoreceptor-specific cell death in the rat retina. Auton. Neurosci. 2005, 120, 46–51.
  64. May, C.A.; Neuhuber, W.; Lütjen-Drecoll, E. Immunohistochemical Classification and Functional Morphology of Human Choroidal Ganglion Cells. Investig. Opthalmol. Vis. Sci. 2004, 45, 361–367.
  65. Schrödl, F.; Brehmer, A.; Neuhuber, W.L. Intrinsic choroidal neurons in the duck eye express galanin. J. Comp. Neurol. 2000, 425, 24–33.
  66. De Hoz, R.; Salazar, J.J.; Ramírez, A.I.; Rojas, B.; Triviño, A.; Ramírez, J.M. Estudio comparativo de la inervación coroidea en el hombre y en el conejo (oryctolagus cuniculus). Arch. Soc. Esp. Oftalmol. 2006, 81, 463–470.
  67. Schroedl, F.; De Stefano, M.E.; Reese, S.; Brehmer, A.; Neuhuber, W.L. Comparative anatomy of nitrergic intrinsic choroidal neurons (ICN) in various avian species. Exp. Eye Res. 2004, 78, 187–196.
  68. Li, C.; Fitzgerald, M.E.; Del Mar, N.; Wang, H.; Haughey, C.; Honig, M.G.; Reiner, A. Role of the superior salivatory nucleus in parasympathetic control of choroidal blood flow and in maintenance of retinal health. Exp. Eye Res. 2021, 206, 108541.
  69. Terenghi, G.; Polak, J.M.; Probert, L.; McGregor, G.P.; Ferri, G.L.; Blank, M.A.; Butler, J.M.; Unger, W.G.; Zhang, A.-Q.; Cole, D.F.; et al. Mapping, quantitative distribution and origin of substance P- and VIP-containing nerves in the Uvea of guinea pig eye. Histochemistry 1982, 75, 399–417.
  70. Nakanome, Y.; Karita, K.; Izumi, H.; Tamai, M. Two types of vasodilatation in cat choroid elicited by electrical stimulation of the short ciliary nerve. Exp. Eye Res. 1995, 60, 37–42.
  71. Gherezghiher, T.; Hey, J.A.; Koss, M.C. Parasympathetic nervous control of intraocular pressure. Exp. Eye Res. 1990, 50, 457–462.
  72. Stjernschantz, J.; Bill, A. Effect of intracranial stimulation of the oculomotor nerve on ocular blood flow in the monkey, cat, and rabbit. Investig. Ophthalmol. Vis. Sci. 1979, 18, 99–103.
  73. Reiner, A.; Erichsen, J.T.; Cabot, J.B.; Evinger, C.; Fitzerald, M.E.C.; Karten, H.J. Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion. Vis. Neurosci. 1991, 6, 451–472.
  74. Lütjen-Drecoll, E. Choroidal innervation in primate eyes. Exp. Eye Res. 2006, 82, 357–361.
  75. Triviño, A.; De Hoz, R.; Rojas, B.; Salazar, J.J.; Ramirez, A.I.; Ramirez, J.M. NPY and TH innervation in human choroidal whole-mounts. Histol. Histopathol. 2005, 20, 393–402.
  76. Klooster, J.; Beckers, H.; Tusscher, T.; Vrensen, G.; Van Der Want, J.; Lamers, W. Sympathetic Innervation of the Rat Choroid: An Autoradiographic Tracing and Immunohistochemical Study. Ophthalmic Res. 1996, 28, 36–43.
  77. Schrödl, F.; Tines, R.; Brehmer, A.; Neuhuber, W.L. Intrinsic choroidal neurons in the duck eye receive sympathetic input: Anatomical evidence for adrenergic modulation of nitrergic functions in the choroid. Cell Tissue Res. 2001, 304, 175–184.
  78. May, C.A. Chronologic versus Biologic Aging of the Human Choroid. Sci. World J. 2013, 2013, 378206.
  79. Jablonski, M.M.; Iannaccone, A.; Reynolds, D.H.; Gallaher, P.; Allen, S.; Wang, X.; Reiner, A. Age-Related Decline in VIP-Positive Parasympathetic Nerve Fibers in the Human Submacular Choroid. Investig. Opthalmol. Vis. Sci. 2007, 48, 479–485.
  80. Nuzzi, R.; Finazzo, C.; Grignolo, F.M. Changes in adrenergic innervation of the choroid during aging. J. Fr. Dophtalmol. 1996, 19, 89–96.
  81. Hoz, A.D.; Ramírez, A.I.; Salazar, J.J.; Rojas, B.; Ramírez, J.M.; Triviño, A. Substance P and calcitonin gene-related peptide intrinsic choroidal neurons in human choroidal whole-mounts. Histol. Histopathol. 2008, 23, 1249–1258.
  82. Sghari, S.; Davies, W.I.L.; Gunhaga, L. Elucidation of Cellular Mechanisms That Regulate the Sustained Contraction and Relaxation of the Mammalian Iris. Investig. Opthalmol. Vis. Sci. 2020, 61, 5.
  83. Lai, J.S.M.; Tham, C.C.Y.; Lam, D.S.C. Comparative study of intraoperative mitomycin C and beta irradiation in pterygium surgery. Br. J. Ophthalmol. 2001, 85, 121–123.
  84. Douglas, R.H. The pupillary light responses of animals; a review of their distribution, dynamics, mechanisms and functions. Prog. Retin. Eye Res. 2018, 66, 17–48.
  85. Gaudric, A.; Coscas, G.; Bird, A. Choroidal Ischemia. Am. J. Ophthalmol. 1982, 94, 489–498.
  86. Reiner, A.; Fitzgerald, M.E.; Del Mar, N.; Li, C. Neural control of choroidal blood flow. Prog. Retin. Eye Res. 2018, 64, 96–130.
  87. Li, C.; Fitzgerald, M.E.C.; Del Mar, N.; Cuthbertson-Coates, S.; LeDoux, M.S.; Gong, S.; Ryan, J.P.; Reiner, A. The identification and neurochemical characterization of central neurons that target parasympathetic preganglionic neurons involved in the regulation of choroidal blood flow in the rat eye using pseudorabies virus, immunolabeling and conventional pathway tracing methods. Front. Neuroanat. 2015, 9, 65.
  88. Tusscher, M.P.T.; Klooster, J.; Baljet, B.; Van der Werf, F.; Vrensen, G.F. Pre- and post-ganglionic nerve fibres of the pterygopalatine ganglion and their allocation to the eyeball of rats. Brain Res. 1990, 517, 315–323.
  89. Cuthbertson, S.; LeDoux, M.S.; Jones, S.; Jones, J.; Zhou, Q.; Gong, S.; Ryan, P.; Reiner, A. Localization of preganglionic neurons that innervate choroidal neurons of pterygopalatine ganglion. Investig. Opthalmol. Vis. Sci. 2003, 44, 3713–3724.
  90. Nilsson, S.F.E.; Bill, A. Vasoactive intestinal polypeptide (VIP): Effects in the eye and on regional blood flows. Acta Physiol. Scand. 1984, 121, 385–392.
  91. Nilsson, S.F. Nitric oxide as a mediator of parasympathetic vasodilation in ocular and extraocular tissues in the rabbit. Investig. Ophthalmol. Vis. Sci. 1996, 37, 2110–2119.
  92. Nilsson, S.F.; Linder, J.; Bill, A. Characteristics of uveal vasodilation produced by facial nerve stimulation in monkeys, cats and rabbits. Exp. Eye Res. 1985, 40, 841–852.
  93. Cuthbertson, S.; Jackson, B.; Toledo, C.; Fitzgerald, M.E.C.; Shih, Y.F.; Zagvazdin, Y.; Reiner, A. Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in pigeons. J. Comp. Neurol. 1997, 386, 273–282.
  94. Reiner, A.; Zagvazdin, Y.; Fitzgerald, M.E. Choroidal blood flow in pigeons compensates for decreases in arterial blood pressure. Exp. Eye Res. 2003, 76, 273–282.
  95. Gamlin, P.; Reiner, A.; Karten, H.J. Substance P-containing neurons of the avian suprachiasmatic nucleus project directly to the nucleus of Edinger-Westphal. Proc. Natl. Acad. Sci. USA 1982, 79, 3891–3895.
  96. Cantwell, E.L.; Cassone, V.M. Chicken suprachiasmatic nuclei: I. Efferent and afferent connections. J. Comp. Neurol. 2006, 496, 97–120.
  97. Cantwell, E.L.; Cassone, V.M. Chicken suprachiasmatic nuclei: II. Autoradiographic and immunohistochemical analysis. J. Comp. Neurol. 2006, 499, 442–457.
  98. Fitzgerald, M.E.C.; Gamlin, P.D.R.; Zagvazdin, Y.; Reiner, A. Central neural circuits for the light-mediated reflexive control of choroidal blood flow in the pigeon eye: A laser Doppler study. Vis. Neurosci. 1996, 13, 655–669.
  99. Reiner, A.; Wong, T.; Nazor, C.; DEL Mar, N.; Fitzgerald, M. Type-specific photoreceptor loss in pigeons after disruption of parasympathetic control of choroidal blood flow by the medial subdivision of the nucleus of Edinger-Westphal. Vis. Neurosci. 2016, 33, E008.
  100. Fischer, A.J.; McKinnon, L.A.; Nathanson, N.M.; Stell, W.K. Identification and localization of muscarinic acetylcholine receptors in the ocular tissues of the chick. J. Comp. Neurol. 1998, 392, 273–284.
  101. Zagvazdin, Y.; Fitzgeraldab, M.E.; Reiner, A. Role of Muscarinic Cholinergic Transmission in Edinger-Westphal Nucleus-induced Choroidal Vasodilation in Pigeon. Exp. Eye Res. 2000, 70, 315–327.
  102. Alm, A.; Bill, A. The Effect of Stimulation of the Cervical Sympathetic Chain on Retinal Oxygen Tension and on Uveal, Retinal and Cerebral Blood Flow in Cats. Acta Physiol. Scand. 1973, 88, 84–94.
  103. Alm, A. The effect of sympathetic stimulation on blood flow through the uvea, retina and optic nerve in monkeys (Macaca irus). Exp. Eye Res. 1977, 25, 19–24.
  104. Li, C.; Fitzgerald, M.E.C.; Del Mar, N.; Haughey, C.; Reiner, A. Defective Choroidal Blood Flow Baroregulation and Retinal Dysfunction and Pathology Following Sympathetic Denervation of Choroid. Investig. Opthalmol. Vis. Sci. 2018, 59, 5032–5044.
  105. Martinez-Camarillo, J.-C.; Spee, C.K.; Chen, M.; Rodriguez, A.; Nimmagadda, K.; Trujillo-Sánchez, G.P.; Hinton, D.R.; Giarola, A.; Pikov, V.; Sridhar, A.; et al. Sympathetic Effects of Internal Carotid Nerve Manipulation on Choroidal Vascularity and Related Measures. Investig. Opthalmol. Vis. Sci. 2019, 60, 4303–4309.
  106. Kiel, J.W.; Lovell, M.O. Adrenergic modulation of choroidal blood flow in the rabbit. Investig. Ophthalmol. Vis. Sci. 1996, 37, 673–679.
  107. Nilsson, S.F.E. Neuropeptide Y (NPY): A vasoconstrictor in the eye, brain and other tissues in the rabbit. Acta Physiol. Scand. 1991, 141, 455–467.
  108. Stjernschantz, J.; Geijer, C.; Bill, A. Electrical stimulation of the fifth cranial nerve in rabbits: Effects on ocular blood flow, extravascular albumin content and intraocular pressure. Exp. Eye Res. 1979, 28, 229–238.
  109. Costagliola, C.; Dell’Omo, R.; Agnifili, L.; Bartollino, S.; Fea, A.M.; Uva, M.G.; Zeppa, L.; Mastropasqua, L. How many aqueous humor outflow pathways are there? Surv. Ophthalmol. 2019, 65, 144–170.
  110. Heermann, S. Neuroanatomie der Sehbahn. Mon. Augenheilkd. 2017, 234, 1327–1333.
  111. May, P.J.; Warren, S.; Bohlen, M.O.; Barnerssoi, M.; Horn, A.K.E. A central mesencephalic reticular formation projection to the Edinger-Westphal nuclei. Brain Struct. Funct. 2015, 221, 4073–4089.
  112. Motlagh, M.; Geetha, R. Physiology, Accommodation. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2021.
  113. May, P.J.; Gamlin, P.D. Is Primate Lens Accommodation Unilaterally or Bilaterally Controlled? Investig. Opthalmol. Vis. Sci. 2020, 61, 5.
  114. Lara-Lacárcel, F.; Marín-Franch, I.; Fernández-Sánchez, V.; Riquelme-Nicolás, R.; López-Gil, N. Objective changes in astigmatism during accommodation. Ophthalmic Physiol. Opt. 2021, 41, 1069–1075.
  115. Gamlin, P.D.; Yoon, K. An area for vergence eye movement in primate frontal cortex. Nat. Cell Biol. 2000, 407, 1003–1007.
  116. Schor, C.M.; Lott, L.A.; Pope, D.; Graham, A.D. Saccades reduce latency and increase velocity of ocular accommodation. Vis. Res. 1999, 39, 3769–3795.
  117. Domínguez-Vicent, A.; Monsálvez-Romín, D.; Del Águila-Carrasco, A.J.; Ferrer-Blasco, T.; Montés-Micó, R. Changes in the anterior chamber during accommodation assessed with a Scheimpflug system. J. Cataract. Refract. Surg. 2014, 40, 1790–1797.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Ophthalmology
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
feipeng wu
View Times: 1.3K
Revisions: 2 times (View History)
Update Date: 19 Jan 2022
Table of Contents
    1000/1000
    Hot Most Recent
    Feedback