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The Journal of Neuroscience, April 18, 2007, 27(16):4443-4451; doi:10.1523/JNEUROSCI.0557-07.2007

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Cellular/Molecular
Activation of TRPA1 Channel Facilitates Excitatory Synaptic Transmission in Substantia Gelatinosa Neurons of the Adult Rat Spinal Cord

Masafumi Kosugi,^1,2 Terumasa Nakatsuka,¹ Tsugumi Fujita,¹ Yasuo Kuroda,² and Eiichi Kumamoto¹

Departments of ¹Physiology and ²Neurology, Faculty of Medicine, Saga University, Saga 849-8501, Japan

Correspondence should be addressed to Terumasa Nakatsuka, Department of Physiology, Faculty of Medicine, Saga University, Saga 849-8501, Japan. Email: nakatsuk{at}cc.saga-u.ac.jp

TRPA1 is expressed in primary sensory neurons and hair cells, and it is proposed to be activated by cold stimuli, mechanical stimuli, or pungent ingredients. However, its role in regulating synaptic transmission has never been documented yet. In the present study, we examined whether activation of the TRPA1 channels affects synaptic transmission in substantia gelatinosa (SG) neurons of adult rat spinal cord slices by using the whole-cell patch-clamp technique. A chief ingredient of mustard oil, allyl isothiocyanate (AITC), superfused for 2 min markedly increased the frequency and amplitude of spontaneous EPSCs (sEPSCs), which was accompanied by an inward current. Similar actions were produced by cinnamaldehyde and allicin. The AITC-induced increases in sEPSC frequency and amplitude were resistant to tetrodotoxin (TTX) and La³⁺, whereas being significantly reduced in extent in a Ca²⁺-free bath solution. In the presence of glutamate receptor antagonists CNQX and AP5, AITC did not generate any synaptic activities. The AITC-induced increases in sEPSC frequency and amplitude were reduced by ruthenium red, whereas being unaffected by capsazepine. AITC also increased the frequency and amplitude of spontaneous inhibitory postsynaptic currents; this AITC action was abolished in the presence of TTX or glutamate receptor antagonists. These results indicate that TRPA1 appears to be localized not only at presynaptic terminals on SG neurons to enhance glutamate release, but also in terminals of primary afferents innervating onto spinal inhibitory interneurons, which make synapses with SG neurons. This central modulation of sensory signals may be associated with physiological and pathological pain sensations.

Key words: channel; presynaptic facilitation; glutamate; patch clamp; pain; spinal cord

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Received Oct. 12, 2006; revised March 12, 2007; accepted March 18, 2007.

Correspondence should be addressed to Terumasa Nakatsuka, Department of Physiology, Faculty of Medicine, Saga University, Saga 849-8501, Japan. Email: nakatsuk{at}cc.saga-u.ac.jp

This article has been cited by other articles:

				W. J. Martin Currying Favor With Central Inhibitory Circuits. Focus on: "Effects of TRPA1 Agonists Mustard Oil and Cinnamaldehyde on Lumbar Wide-Dynamic Range Neuronal Responses to Innocuous and Noxious Cutaneous Stimuli in Rats" J Neurophysiol, February 1, 2008; 99(2): 409 - 410. [Full Text] [PDF]

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