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Cold Thermoreceptors, Unexpected Players in Tear Production and Ocular Dryness Sensations

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Cold Thermoreceptors, Unexpected Players in Tear Production and Ocular Dryness Sensations New Developments Cold Thermoreceptors, Unexpected Players in Tear Production and Ocular Dryness Sensations Carlos Belmonte1,2 and Juana Gallar1 hysical and chemical agents acting on the ocular surface Polymodal nociceptor neurons are the most abundant class P(extreme environmental temperatures, wind, foreign bod- of ocular nociceptor neuron. Polymodal nerve endings are ies, and chemicals) elicit conscious sensations and reflex motor activated tonically by mechanical forces, but they also dis- and autonomic responses (blinking, lacrimation, conjunctival charge repeatedly in response to heat, external irritant chem- vasodilation) aimed at protecting the eye from further injury. icals, and a large variety of endogenous chemical agents re- Sensory nerve terminals of trigeminal ganglion neurons inner- leased by damaged tissues and immune cells (protons, vating the cornea and conjunctiva are the origin of the periph- arachidonic acid metabolites, kinins, cytokines, and growth eral neural information that reaches higher central nervous factors) during injury and inflammation.5–8 A prominent fea- system areas, evoking ultimately these protective neural re- ture of polymodal nociceptor neurons is their functional plas- sponses.1–4 ticity after injury. Their responsiveness changes drastically a The innervation of the eye surface is provided by function- few minutes after tissue damage, that is, they develop sensiti- ally distinct types of trigeminal ganglion neurons, whose pe- zation. Sensitizing polymodal nociceptors develop an irregular, ripheral nerve endings specialize in the preferential detection low-frequency impulse activity long after stimulation has of various modalities of physical (mechanical, thermal) and ceased. Also, the threshold for subsequent stimuli decreases, chemical (exogenous irritants and endogenous mediators) and their responses to new stimuli increases.5,6 Sensitization of stimuli, encoding their spatial and temporal characteristics the polymodal nociceptors that innervate injured and/or in- (intensity and duration) into a discharge of nerve impulses. flamed ocular tissues is the origin of spontaneous pain and of Most ocular trigeminal ganglion neurons belong to the general enhanced pain in response to stimuli at the injured area (pri- group of nociceptor sensory neurons whose peripheral nerve mary hyperalgesia).5 When nociceptor nerve endings are di- endings are activated by injurious or near injurious stimuli that rectly damaged, they may exhibit a reduced responsiveness to 5 initiate normal pain sensations. natural stimuli.9,10 Nonetheless, the injured parent axons still display ongoing activity that causes spontaneous pain referred to the wounded area.5,10 Sustained stimulation and/or destruc- CORNEAL PAIN IS SIGNALED BY MECHANO- AND tion of the terminal part of peripheral nerves additionally POLYMODAL NOCICEPTORS trigger long-term molecular and morphologic changes in the surviving segments of polymodal nociceptor neurons. As a Mechanonociceptor neurons are the fastest conducting of the consequence, membrane excitability and responsiveness to nociceptor neurons that innervate the eye surface. Their pe- peripheral stimuli are altered.10 Knowledge of the molecular ripheral endings are normally recruited only by mechanical substrates responsible for polymodality and plasticity after in- forces and respond to sustained mechanical stimulation with a flammation or nerve damage has progressed in recent years, short burst of nerve impulses at intensities that are compara- leading to the identification of a large number of transducing tively low relative to those that cause injury in other territories and receptor membrane proteins such as TRP channels and such as the skin, but become potentially noxious for the receptor molecules for inflammatory agents, as well as to a fragile, unkeratinized corneal or conjunctival surface epithe- more detailed definition of the intracellular signaling pathways lium. This population of ocular sensory nerve afferents appears and gene expression changes associated with injury.11 to signal primarily mechanical insults to the eye surface and Postinjury modifications of the impulse firing pattern in possibly contributes to the sharp, pricking pain experienced polymodal nociceptors and of their responsiveness to new when a foreign body touches the corneal or conjunctival sur- stimuli are determined by the intensity, type, time course, and face.6,7 duration of the tissue insult. This variability explains in mech- anistic terms the differences in intensity profile and temporal evolution of ocular discomfort and pain sensations that de- 1 velop under pathological conditions involving cell destruction, From the Instituto de Neurociencias de Alicante, Universidad local inflammation, and/or peripheral nerve injury of the eye Miguel Herna´ndez-CSIC (Consejo Superior de Investigaciones Científi- 5,9 cas), San Juan de Alicante, Spain; and the 2Fundacio´n de Investigacio´n surface tissues. As expected from their nociceptive nature, Oftalmolo´gica, Instituto de Oftalmología Ferna´ndez-Vega, Oviedo, experimental, selective stimulation of the population of cor- Spain. neal polymodal nociceptors in humans evokes stinging and Supported by the Spanish MICINN (Ministerio de Ciencia e Inno- burning pain referred to the eye.12–15 Moreover, drugs that vacio´n): projects BFU2008-04425 (CB) and SAF2008-00529 (JG), and interfere with inflammation pathways thereby reducing noci- by Consolider-Ingenio 2010 CSD2007-00023. ceptor sensitization behave as efficacious analgesics. There- Submitted for publication December 23, 2009; revised February 3, fore, it is generally accepted that activity in polymodal nocice- 2011; accepted March 25, 2011. ptors at the ocular surface is the main basis of the pain that Disclosure: C. Belmonte, None; J. Gallar, None Corresponding author: Carlos Belmonte, Instituto de Neurocien- accompanies clinical conditions such as keratitis, corneal ul- cias de Alicante, Universidad Miguel Hernandez-CSIC, Avda. Santiago cers, surgical wounds, contact lens wear, and conjunctivitis. Ramo´n y Cajal s/n, 03550 San Juan de Alicante, Spain; Likewise, the prevalent opinion concerning the origin of the [email protected]. unpleasant sensations that accompany dry eye has been that DOI:10.1167/iovs.09-5119 3888 Investigative Ophthalmology & Visual Science, May 2011, Vol. 52, No. 6 Copyright 0 The Association for Research in Vision and Ophthalmology, Inc. Downloaded from iovs.arvojournals.org on 10/01/2021 IOVS, May 2011, Vol. 52, No. 6 Ocular Dryness and Corneal Cold Receptors 3889 they are primarily due to mechanical and/or chemical excita- wild-type animals. This strongly supports the view that under tion of polymodal nociceptors secondary to distortion of nerve normal circumstances, the continuous impulse firing from cold endings by ocular surface desiccation, tear hyperosmolarity, thermoreceptors represents a tonic stimulus for basal tear fluid and/or release of inflammatory mediators into tears.1–3 secretion, conceivably activating at the superior salivary nu- cleus the parasympathetic secretory drive to the lacrimal glands and goblet cells (Fig. 1).26,27 Moreover, experimental THE CORNEA IS ALSO INNERVATED BY warming of the ocular surface in mice or human subjects—a COLD THERMORECEPTORS maneuver that transiently silences corneal cold thermorecep- tors—decreases basal tearing, further confirming in humans Cold thermoreceptors represent a separate class of corneocon- the hypothesis that the basal flow of tears is partly dependent junctival sensory neurons with unique, specific properties. on the tonic input from the peripheral cold thermoreceptor These include spontaneous firing of nerve impulses, often in endings located at the ocular surface.18 bursts, at the normal background temperature of the cornea or The activity of cold thermoreceptors within the normal conjunctiva (34–35°C) and immediate increase of their im- range of corneal temperatures in healthy eyes appears to pulse activity when the corneal temperature drops, which exert a nearly maximal stimulatory effect on tear secretion, thereafter stabilizes gradually at a higher impulse frequency because further increases in cold receptor activity obtained level, proportional to the new value of corneal temperature.16 by larger corneal cooling stimuli within the innocuous level Thus, cold thermoreceptors encode in their firing frequency causes only modest elevations of the basal tearing rate.18 the speed and magnitude of temperature reductions at the However, it is worth noting that the magnitude of the tonic ocular surface as well as the final static temperature. In the excitatory input of cold receptors to central parasympa- normal range of corneal temperatures (36–29°C), cold thermo- thetic neurons possibly depends on the total number of receptors are able to discriminate transient temperature varia- active fibers and their mean firing frequency, as occurs with tions of 0.5°C or less.7,17,18 As expected, psychophysical ex- other secretory and vascular autonomic responses driven by periments using corneal esthesiometry in human subjects have cutaneous thermoreceptor sensory input.28,29 Cold- shown that they are able to discriminate corneal temperature dependent basal tearing is expected to decay if the overall drops of 1°C to 2°C below basal level.14,15 sensory inflow provided by the whole population of ocular The prominent sensitivity of ocular cold receptors to small cold afferent fibers decreases, as presumably occurs when temperature reductions of the
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