Corneal dry-responsive neurons in the spinal trigeminal nucleus respond to innocuous cooling in the rat

Journal of Neurophysiology

Volumn 109, Issue 10, 2013, Pages 2517-2522

  Kurose, Masayuki ^a   Meng, Ian D ^b  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b UNIVERSITY OF NEW ENGLAND   (United States)

Author keywords

Cornea; Eye; Nociception; Trigeminal

Indexed keywords

ARTIFICIAL TEAR; MENTHOL;

ANIMAL EXPERIMENT; ARTICLE; BRAIN STEM; COOLING; CORNEA CELL; DRY RESPONSIVE NEURON; EVOKED RESPONSE; LACRIMATION; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; SENSORY NERVE; STIMULATION; THERMAL STIMULATION; TISSUE INJURY; TRIGEMINAL NUCLEUS;

CORNEA; EYE; NOCICEPTION; TRIGEMINAL;

ACIDS; ACTION POTENTIALS; ANIMALS; BRAIN STEM; COLD TEMPERATURE; CORNEA; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; MALE; MENTHOL; NEURONS, AFFERENT; NOCICEPTION; OPHTHALMIC SOLUTIONS; OSMOSIS; RATS; RATS, SPRAGUE-DAWLEY; TRIGEMINAL NUCLEUS, SPINAL;

EID: 84878530689     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00889.2012     Document Type: Article

References (33)

1. Acosta MC, Belmonte C, Gallar J. Sensory experiences in humans and single-unit activity in cats evoked by polymodal stimulation of the cornea. J Physiol 534: 511-525, 2001a.
2. Acosta MC, Peral A, Luna C, Pintor J, Belmonte C, Gallar J. Tear secretion induced by selective stimulation of corneal and conjunctival sensory nerve fibers. Invest Ophthalmol Vis Sci 45: 2333-2336, 2004.
3. Acosta MC, Tan ME, Belmonte C, Gallar J. Sensations evoked by selective mechanical, chemical, and thermal stimulation of the conjunctiva and cornea. Invest Ophthalmol Vis Sci 42: 2063-2067, 2001b.
4. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208, 2007.
5. Belmonte C, Aracil A, Acosta MC, Luna C, Gallar J. Nerves and sensations from the eye surface. Ocul Surf 2: 248-253, 2004.
6. Belmonte C, Gallar J. Cold thermoreceptors, unexpected players in tear production and ocular dryness sensations. Invest Ophthalmol Vis Sci 52: 3888-3892, 2011.
7. Brock JA, Pianova S, Belmonte C. Differences between nerve terminal impulses of polymodal nociceptors and cold sensory receptors of the guinea-pig cornea. J Physiol 533: 493-501, 2001.
8. Cabanes C, Viana F, Belmonte C. Differential thermosensitivity of sensory neurons in the guinea pig trigeminal ganglion. J Neurophysiol 90: 2219-2231, 2003.
9. Carr RW, Pianova S, Fernandez J, Fallon JB, Belmonte C, Brock JA. Effects of heating and cooling on nerve terminal impulses recorded from cold-sensitive receptors in the guinea-pig cornea. J Gen Physiol 121: 427-439, 2003.
10. 2 stimulation of the cornea: a comparison between human sensation and nerve activity in polymodal nociceptive afferents of the cat. Eur J Neurosci 7: 1154-1163, 1995.
11. de la Pena E, Malkia A, Cabedo H, Belmonte C, Viana F. The contribution of TRPM8 channels to cold sensing in mammalian neurones. J Physiol 567: 415-426, 2005.
12. Gallar J, Pozo MA, Tuckett RP, Belmonte C. Response of sensory units with unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat's cornea. J Physiol 468: 609-622, 1993.
13. Henriquez VM, Evinger C. The three-neuron corneal reflex circuit and modulation of second-order corneal responsive neurons. Exp Brain Res 179: 691-702, 2007.
14. Hirata H, Meng ID. Cold-sensitive corneal afferents respond to a variety of ocular stimuli central to tear production: implications for dry eye disease. Invest Ophthalmol Vis Sci 51: 3969-3976, 2010.
15. Hirata H, Okamoto K, Tashiro A, Bereiter DA. A novel class of neurons at the trigeminal subnucleus interpolaris/caudalis transition region monitors ocular surface fluid status and modulates tear production. J Neurosci 24: 4224-4232, 2004.
16. Hirata H, Takeshita S, Hu JW, Bereiter DA. Cornea-responsive medullary dorsal horn neurons: modulation by local opioids and projections to thalamus and brain stem. J Neurophysiol 84: 1050-1061, 2000.
17. Madrid R, Donovan-Rodriguez T, Meseguer V, Acosta MC, Belmonte C, Viana F. Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J Neurosci 26: 12512-12525, 2006.
18. Marfurt CF, Del Toro DR. Corneal sensory pathway in the rat: a horseradish peroxidase tracing study. J Comp Neurol 261: 450-459, 1987.
19. McCoy DD, Knowlton WM, McKemy DD. Scraping through the ice: uncovering the role of TRPM8 in cold transduction. Am J Physiol Regul Integr Comp Physiol 300: R1278-R1287, 2011.
20. McKemy DD, Neuhausser WM, Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58, 2002.
21. Meng ID, Bereiter DA. Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea. Neuroscience 72: 243-254, 1996.
22. Meng ID, Hu JW, Benetti AP, Bereiter DA. Encoding of corneal input in two distinct regions of the spinal trigeminal nucleus in the rat: cutaneous receptive field properties, responses to thermal and chemical stimulation, modulation by diffuse noxious inhibitory controls, and projections to the parabrachial area. J Neurophysiol 77: 43-56, 1997.
23. Meng ID, Hu JW, Bereiter DA. Differential effects of morphine on corneal-responsive neurons in rostral versus caudal regions of spinal trigeminal nucleus in the rat. J Neurophysiol 79: 2593-2602, 1998.
24. Nealen ML, Gold MS, Thut PD, Caterina MJ. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90: 515-520, 2003.
25. Parra A, Madrid R, Echevarria D, del Olmo S, Morenilla-Palao C, Acosta MC, Gallar J, Dhaka A, Viana F, Belmonte C. Ocular surface wetness is regulated by TRPM8-dependent cold thermoreceptors of the cornea. Nat Med 16: 1396-1399, 2010.
26. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A. A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715, 2002.
27. Robbins A, Kurose M, Winterson BJ, Meng ID. Menthol activation of corneal cool cells induces TRPM8-mediated lacrimation but not nociceptive responses in rodents. Invest Ophthalmol Vis Sci 53: 7034-7042, 2012.
28. Strassman AM, Vos BP. Somatotopic and laminar organization of fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J Comp Neurol 331: 495-516, 1993.
29. Tanelian DL, Beuerman RW. Responses of rabbit corneal nociceptors to mechanical and thermal stimulation. Exp Neurol 84: 165-178, 1984.
30. Tashiro A, Okamoto K, Chang Z, Bereiter DA. Behavioral and neurophysiological correlates of nociception in an animal model of photokeratitis. Neuroscience 169: 455-462, 2010.
31. Thut PD, Wrigley D, Gold MS. Cold transduction in rat trigeminal ganglia neurons in vitro. Neuroscience 119: 1071-1083, 2003.
32. Toth IE, Boldogkoi Z, Medveczky I, Palkovits M. Lacrimal preganglionic neurons form a subdivision of the superior salivatory nucleus of rat: transneuronal labelling by pseudorabies virus. J Auton Nerv Syst 77: 45-54, 1999.
33. Zanotto KL, Merrill AW, Carstens MI, Carstens E. Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli. J Neurophysiol 97: 966-978, 2007.