NMDA Receptor Blockade Reduces Temporomandibular Joint-evoked Activity of Trigeminal Subnucleus Caudalis Neurons in an Estrogen-dependent Manner

Overview

Journal Neuroscience

Specialty Neurology

Date 2009 Oct 6

PMID 19799971

Citations 4

Authors

A Tashiro

K Okamoto

D A Bereiter

Affiliations

Soon will be listed here.

Abstract

Estrogen status is a risk factor in painful temporomandibular disorders (TMJD). Previously we reported that estradiol (E2) enhanced nociceptive processing of TMJ input by neurons in superficial laminae at the spinomedullary (Vc/C(1-2)) region; however, the mechanisms for this enhancement are not known. The present study determined if ionotropic glutamate receptors contribute to TMJ nociceptive processing in an E2-dependent manner. Ovariectomized (OvX) female rats were treated with high E2 (HE2) or low dose E2 (LE2) for 2 days and neural activity was recorded in laminae I-II at the Vc/C(1-2) region. TMJ-responsive units were activated by ATP injections into the joint space. ATP-evoked unit responses in HE2 rats were reduced significantly by topical application of the N-methyl-D-aspartate receptor antagonist, D(-)-2-amino-5-phosphonopentanoic acid (AP5) in a dose-related manner, while units from LE2 were not affected. Application of the non-NMDA receptor antagonist, 6,7-dinitroquinoxaline-2,3-dione (DNQX), inhibited the ATP-evoked responses in both groups. Spontaneous activity of TMJ units was not influenced by AP5, whereas it was reduced by DNQX similarly in both groups. The high threshold convergent cutaneous receptive field area of TMJ units was not changed by AP5, whereas DNQX caused a significant reduction in both groups. These results suggest that NMDA-dependent mechanisms contribute to the enhanced ATP-evoked responses of TMJ units in superficial laminae at the Vc/C(1-2) region under high E2 conditions, while non-NMDA-dependent mechanisms modify the encoding properties of TMJ units independent of E2 status.

Citing Articles

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GABAergic influence on temporomandibular joint-responsive spinomedullary neurons depends on estrogen status.

Tashiro A, Bereiter D, Thompson R, Nishida Y Neuroscience. 2013; 259:53-62.

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References

Tashiro A, Okamoto K, Milam S, Bereiter D . Differential effects of estradiol on encoding properties of TMJ units in laminae I and V at the spinomedullary junction in female rats. J Neurophysiol. 2007; 98(6):3242-53. DOI: 10.1152/jn.00677.2007. View

Ayesh E, Jensen T, Svensson P . Effects of intra-articular ketamine on pain and somatosensory function in temporomandibular joint arthralgia patients. Pain. 2007; 137(2):286-294. DOI: 10.1016/j.pain.2007.09.004. View

McEwen B . Estrogen actions throughout the brain. Recent Prog Horm Res. 2002; 57:357-84. DOI: 10.1210/rp.57.1.357. View

Woolley C . Effects of estrogen in the CNS. Curr Opin Neurobiol. 1999; 9(3):349-54. DOI: 10.1016/s0959-4388(99)80051-8. View

Foy M . 17beta-estradiol: effect on CA1 hippocampal synaptic plasticity. Neurobiol Learn Mem. 2001; 76(3):239-52. DOI: 10.1006/nlme.2001.4018. View

Shinoda M, Ozaki N, Asai H, Nagamine K, Sugiura Y . Changes in P2X3 receptor expression in the trigeminal ganglion following monoarthritis of the temporomandibular joint in rats. Pain. 2005; 116(1-2):42-51. DOI: 10.1016/j.pain.2005.03.042. View

Schaible H . Spinal mechanisms contributing to joint pain. Novartis Found Symp. 2004; 260:4-22. View

Shigenaga Y, Sera M, Nishimori T, Suemune S, Nishimura M, Yoshida A . The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol. 1988; 268(4):489-507. DOI: 10.1002/cne.902680403. View

Luccarini P, Sessle B, Woda A . Superficial and deep convergent nociceptive neurons are differentially affected by N-methyl-D-aspartate applied on the brainstem surface of the rat medullary dorsal horn. Neuroscience. 2001; 107(2):311-6. DOI: 10.1016/s0306-4522(01)00360-8. View

10.

LeResche L, Mancl L, Sherman J, Gandara B, Dworkin S . Changes in temporomandibular pain and other symptoms across the menstrual cycle. Pain. 2003; 106(3):253-261. DOI: 10.1016/j.pain.2003.06.001. View

11.

Takeuchi Y, Toda K . Subtypes of nociceptive units in the rat temporomandibular joint. Brain Res Bull. 2003; 61(6):603-8. DOI: 10.1016/s0361-9230(03)00219-3. View

12.

Bereiter D, Bereiter D . N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor antagonism reduces Fos-like immunoreactivity in central trigeminal neurons after corneal stimulation in the rat. Neuroscience. 1996; 73(1):249-58. DOI: 10.1016/0306-4522(96)00038-3. View

13.

Antal M, Fukazawa Y, Eordogh M, Muszil D, Molnar E, Itakura M . Numbers, densities, and colocalization of AMPA- and NMDA-type glutamate receptors at individual synapses in the superficial spinal dorsal horn of rats. J Neurosci. 2008; 28(39):9692-701. PMC: 3844880. DOI: 10.1523/JNEUROSCI.1551-08.2008. View

14.

HAMILTON S, McMahon S . ATP as a peripheral mediator of pain. J Auton Nerv Syst. 2000; 81(1-3):187-94. DOI: 10.1016/s0165-1838(00)00137-5. View

15.

Okamoto K, Hirata H, Takeshita S, Bereiter D . Response properties of TMJ units in superficial laminae at the spinomedullary junction of female rats vary over the estrous cycle. J Neurophysiol. 2003; 89(3):1467-77. DOI: 10.1152/jn.00795.2002. View

16.

Liu H, Wang H, Sheng M, Jan L, Jan Y, Basbaum A . Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci U S A. 1994; 91(18):8383-7. PMC: 44610. DOI: 10.1073/pnas.91.18.8383. View

17.

Cairns B, Sessle B, Hu J . Characteristics of glutamate-evoked temporomandibular joint afferent activity in the rat. J Neurophysiol. 2001; 85(6):2446-54. DOI: 10.1152/jn.2001.85.6.2446. View

18.

Seagrove L, Suzuki R, Dickenson A . Electrophysiological characterisations of rat lamina I dorsal horn neurones and the involvement of excitatory amino acid receptors. Pain. 2004; 108(1-2):76-87. DOI: 10.1016/j.pain.2003.12.004. View

19.

Isselee H, De Laat A, De Mot B, Lysens R . Pressure-pain threshold variation in temporomandibular disorder myalgia over the course of the menstrual cycle. J Orofac Pain. 2002; 16(2):105-17. View

20.

Fillingim R, Maixner W, Kincaid S, Sigurdsson A, Harris M . Pain sensitivity in patients with temporomandibular disorders: relationship to clinical and psychosocial factors. Clin J Pain. 1996; 12(4):260-9. DOI: 10.1097/00002508-199612000-00005. View