Potassium-dependent prolonged field bursts in the dentate gyrus: Effects of extracellular calcium and amino acid receptor antagonists

Abstract

The dentate gyrus in rat hippocampal slices produces spontaneous, prolonged bursts of population spikes (i.e. prolonged field bursts) when [Ca 2+] 0 is lowered (0-0.5 mM) and [K +] 0 is concurrently elevated (9–11 mM). In this investigation we examined whether the dentate gyrus could also generate spontaneous field bursts in relatively “normal” (i.e. nominal 1.3 mM) or only moderately decreased [Ca 2+] 0 (i.e. nominal 0.9 mM). In 1.3 mM [Ca 2+] 0, no prolonged field bursts occurred spontaneously in the dentate gyrus when [K +] 0 was raised as high as 12 mM. Prolonged field bursts were generated, however, when [K +] 0 was further increased to 13–15 mM. Similar bursts could be generated at [K +] 0 within the “physiological ceiling level” observed in vivo during seizure activity (i.e. 11–12 mM) if: (i) the bath [Ca 2+] was reduced to 0.9 mM; or (ii) the GABA type A-receptor antagonist bicuculline was added in the presence of “normal” (1.3 mM) [Ca 2+] 0. Adding both the N-methyl- d-aspartate and non N-methyl- d-aspartate receptor antagonists, (±)-2-amino-5-phosphonopentanoic acid (50–100 μM) and 6,7-dinitroquinoxaline-2,3-dione (50–100 μM), respectively, did not block the occurrence of the field bursts. The bursts generated in 1.3 mM [Ca 2+] 0, 12 mM [K +] 0, bicuculline, (±)-2-amino-5-phosphonopen-tanoic acid and 6,7-dinitroquinoxaline-2,3-dione could, however, be reversibly depressed or blocked if [Ca 2+] 0 was raised to 2.0 mM. These data suggest that: (i) the dentate gyrus (like CA1) can produce prolonged field bursts in “normal” [Ca 2+] 0 when [K +] 0 is elevated, although the [K +] 0 threshold is higher; (ii) the dentate gyrus can generate prolonged field bursts in response to [K +] 0 elevations within the physiological ceiling, provided [Ca 2+] 0 is moderately lowered (i.e. 0.9 mM) or GABA type A-transmission is blocked; and (iii) antagonists of excitatory amino acid-mediated neurotransmission do not block the prolonged field bursts produced under any of these conditions.