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Two distinct oscillatory states determined by the NMDA receptor in rat inferior olive

Dimitris G. Placantonakis and John P. Welsh

1. The effects of N-methyl-D-aspartate (NMDA) receptor activation and blockade on subthreshold membrane potential oscillations of inferior olivary neurones were studied in brainstem slices from 12- to 21-day-old rats.
2. Dizocilpine (MK-801), a non-competitive NMDA antagonist, at 1-45 µM abolished spontaneous subthreshold oscillations, without affecting membrane potential, input resistance, or the low-threshold calcium current, I_T. Ketamine (100 µM), a non-competitive NMDA antagonist, and L-689,560 (20 µM), an antagonist at the glycine site of the NMDA receptor, also abolished the oscillations, while the competitive non-NMDA antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 20-50 µM) had no effect.
3. NMDA (100 µM) induced 4.1 Hz subthreshold oscillations and reversibly depolarized olivary neurones by 13.7 mV. In contrast, 10 µM -amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) and 20 µM kainic acid depolarized the membrane equivalently but did not induce oscillations.
4. Both NMDA-induced and spontaneous subthreshold oscillations were unaffected by 1 µM tetrodotoxin and were prevented by substituting extracellular calcium with cobalt.
5. Removing magnesium from the perfusate did not affect spontaneous subthreshold oscillations but did prevent NMDA-induced oscillations.
6. NMDA-induced oscillations were resistant to 50 µM mibefradil, an I_T blocker, in contrast to spontaneous oscillations. Both oscillations were inhibited by 20 µM nifedipine, an L-type calcium channel antagonist, and 200 nM -agatoxin IVA, a P-type calcium channel blocker. Bay K 8644 (10 µM), an L-type Ca²⁺ agonist, significantly enhanced the amplitude of both spontaneous and NMDA-induced oscillations.
7. The data indicate that NMDA receptor activation induces olivary neurones to manifest high amplitude membrane potential oscillations in part mediated by L- and P- but not T-type calcium currents. Moreover, the data demonstrate that NMDA receptor currents are necessary for generation of spontaneous subthreshold oscillations in the inferior olive.

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