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The Journal of Neuroscience, September 9, 2009, 29(36):11161-11171; doi:10.1523/JNEUROSCI.3365-09.2009

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Behavioral/Systems/Cognitive
Astroglia in Medullary Dorsal Horn (Trigeminal Spinal Subnucleus Caudalis) Are Involved in Trigeminal Neuropathic Pain Mechanisms

Akiko Okada-Ogawa,^1,2 Ikuko Suzuki,³ Barry J. Sessle,^5,6 Chen-Yu Chiang,⁵ Michael W. Salter,^5,6,7 Jonathan O. Dostrovsky,^5,6 Yoshiyuki Tsuboi,^3,4 Masahiro Kondo,^3,4 Junichi Kitagawa,^3,4 Azusa Kobayashi,^1,2 Noboru Noma,^1,2 Yoshiki Imamura,^1,2 and Koichi Iwata^3,4,8

¹Department of Oral Diagnosis, ²Division of Oral Health Science, Dental Research Center, ³Department of Physiology, and ⁴Division of Functional Morphology, Dental Research Center, Nihon University School of Dentistry, Chiyoda-ku, Tokyo 101-8310, Japan, ⁵Faculty of Dentistry, University of Toronto, Toronto, Ontario M5G 1G6, Canada, ⁶Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A8, Canada, ⁷Program in Neuroscience and Mental Health, Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada, and ⁸Division of Applied System Neuroscience, Advanced Medical Research Center, Nihon University Graduate School of Medical Science, Itabashi-ku, Tokyo 173-8610, Japan

Correspondence should be addressed to Dr. Koichi Iwata, Department of Physiology, Nihon University School of Dentistry, 1-8-13 Kanda-Surugadai, Chiyoda-ku, Tokyo 101-8310, Japan. Email: iwata-k{at}dent.nihon-u.ac.jp

The aim of this study was to investigate whether astroglia in the medullary dorsal horn (trigeminal spinal subnucleus caudalis; Vc) may be involved in orofacial neuropathic pain following trigeminal nerve injury. The effects of intrathecal administration of the astroglial aconitase inhibitor sodium fluoroacetate (FA) were tested on Vc astroglial hyperactivity [as revealed by glial fibrillary acid protein (GFAP) labeling], nocifensive behavior, Vc extracellular signal-regulated kinase phosphorylation (pERK), and Vc neuronal activity in inferior alveolar nerve-transected (IANX) rats. Compared with sham-control rats, a significant increase occurred in GFAP-positive cells in ipsilateral Vc at postoperative day 7 in IANX rats, which was prevented following FA administration. FA significantly increased the reduced head withdrawal latency to high-intensity heat stimulation of the maxillary whisker pad skin in IANX rats, although it did not significantly affect the reduced escape threshold to low-intensity mechanical stimulation of the whisker skin in IANX rats. FA also significantly reduced the increased number of pERK-like immunoreactive cells in Vc and the enhanced Vc nociceptive neuronal responses following high-intensity skin stimulation that were documented in IANX rats, and glutamine administration restored the enhanced responses. These various findings provide the first documentation that astroglia is involved in the enhanced nociceptive responses of functionally identified Vc nociceptive neurons and in the associated orofacial hyperalgesia following trigeminal nerve injury.

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Received July 14, 2009; accepted July 27, 2009.

Correspondence should be addressed to Dr. Koichi Iwata, Department of Physiology, Nihon University School of Dentistry, 1-8-13 Kanda-Surugadai, Chiyoda-ku, Tokyo 101-8310, Japan. Email: iwata-k{at}dent.nihon-u.ac.jp

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