SYNCHRONOUS BURSTING IN A SUBSET OF INTERNEURONS INHIBITORY TO THE GOLDFISH MAUTHNER CELL - SYNAPTIC MEDIATION AND PLASTICITY

1. Presynaptic activity in the inhibitory network impinging on the Mau thner (M-) cell was investigated in the goldfish medulla in vivo using extra- and intracellular recordings. The inhibitory presynaptic volle y elicited by stimulation of the contralateral vestibular nerve consis ted of multiple successive peaks at high frequency (up to 1,000 Hz). L ess pronounced multicomponent responses were recorded after antidromic activation of the M-cell. Such high-frequency ''oscillatory'' held po tentials also occurred spontaneously. 2. In intracellular recordings, a subset of inhibitory interneurons showed evoked and spontaneous burs t discharge. Burst action potentials were correlated with the peaks in the extracellular volley, suggesting that repetitive firing of these cells is synchronized. Nonbursting cells, on the other hand, fired sin gle action potentials in response to vestibular stimuli and were not a ctivated via the M-cell collateral network. 3. Bursting cells were det ermined morphologically to be part of the feedback inhibitory circuit. Their responses to stimulation of the contralateral vestibular nerve thus suggest the existence of a crossed excitatory pathway to these in terneurons. 4. Vestibular-evoked excitatory postsynaptic potentials( E PSPs) in bursting interneurons had a short latency of 0.781 +/- 0.08 m s (mean +/- SD, n = 18) but reached threshold at 2.25 +/- 1 ms (n = 21 ). These characteristics are suggestive of a chemically mediated EPSP. Indeed, the evoked synchronous repetitive activity of these cells was prevented by superfusion with excitatory amino-acid receptor antagoni sts. 5. Bursting neurons showed several characteristics that different iate them from nonbursting cells, including brief action potentials, p lateau responses, and intense spontaneous subthreshold activity. 6. Wi th extracellular recordings, tetanization of contralateral vestibular primary afferents evoked a long-lasting potentiation of oscillatory po pulation responses in 11 of 27 cases. Furthermore in three experiments , the frequency of occurrence of spontaneous bursts was enhanced and a similar facilitation was detected at the intracellular level. 7. We c onclude that a subset of interneurons in this inhibitory network is ca pable of repetitive discharges and that evoked as well as spontaneous firing in this population is synchronized. Although electrical couplin g between interneurons may mediate synchronization and intrinsic membr ane properties may promote burst activity, our data suggest strongly t hat repetitive firing requires chemically mediated transmission. Furth ermore they indicate that the mechanisms underlying evoked as well as spontaneous bursting in this population show activity-dependent plasti city.