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The Journal of Neuroscience, February 8, 2006, 26(6):1787-1794; doi:10.1523/JNEUROSCI.4856-05.2006

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Behavioral/Systems/Cognitive
Direct GABAergic and Glycinergic Inhibition of the Substantia Gelatinosa from the Rostral Ventromedial Medulla Revealed by In Vivo Patch-Clamp Analysis in Rats

Go Kato,^1,2 Toshiharu Yasaka,¹ Toshihiko Katafuchi,¹ Hidemasa Furue,¹ Masaharu Mizuno,³ Yukihide Iwamoto,² and Megumu Yoshimura¹

¹Departments of Integrative Physiology and ²Orthopedic Surgery, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan, and ³Division of Higher Brain Functions, Department of Brain Science and Engineering, Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, Kitakyushu 808-0196, Japan

Correspondence should be addressed to Toshihiko Katafuchi, Department of Integrative Physiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan. Email: kataf{at}physiol.med.kyushu-u.ac.jp

Stimulation of the rostral ventromedial medulla (RVM) is believed to exert analgesic effects through the activation of the serotonergic system descending to the spinal dorsal horn; however, how nociceptive transmission is modulated by the descending system has not been fully clarified. To investigate the inhibitory mechanisms affected by the RVM, an in vivo patch-clamp technique was used to record IPSCs from the substantia gelatinosa (SG) of the spinal cord evoked by chemical (glutamate injection) and electrical stimulation (ES) of the RVM in adult rats. In the voltage-clamp mode, the RVM glutamate injection and RVM-ES produced an increase in both the frequency and amplitude of IPSCs in SG neurons that was not blocked by glutamate receptor antagonists. Serotonin receptor antagonists were unexpectedly without effect, but a GABA_A receptor antagonist, bicuculline, or a glycine receptor antagonist, strychnine, completely suppressed the RVM stimulation-induced increase in IPSCs. The RVM-ES-evoked IPSCs showed fixed latency and no failure at 20 Hz stimuli with a conduction velocity of >3 m/s (3.1–20.7 m/s), suggesting descending monosynaptic GABAergic and/or glycinergic inputs from the RVM to the SG through myelinated fibers. In the current-clamp mode, action potentials elicited by noxious mechanical stimuli applied to the receptive field of the ipsilateral hindlimb were suppressed by the RVM-ES in more than half of the neurons tested (63%; 10 of 16). These findings suggest that the RVM-mediated antinociceptive effects on noxious inputs to the SG may be exerted preferentially by the direct GABAergic and glycinergic pathways to the SG.

Key words: descending inhibitory system; in vivo patch clamp; substantia gelatinosa; pain; GABA; glycine

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Received Nov. 10, 2005; revised Dec. 23, 2005; accepted Dec. 26, 2005.

Correspondence should be addressed to Toshihiko Katafuchi, Department of Integrative Physiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan. Email: kataf{at}physiol.med.kyushu-u.ac.jp

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