Transient Enhancement of Spike-Evoked Calcium Signaling by a Serotonergic Interneuron

Enhancement of presynaptic Ca2+ signals is widely recognized as a potential mechanism for heterosynaptic potentiation of neurotransmitter release. Here we show that stimulation of a serotonergic interneuron increased spike-evoked Ca2+ in a manner consistent with its neuromodulatory effect on synaptic transmission. In the gastropod mollusk, Tritonia diomedea, stimulation of a serotonergic dorsal swim interneuron (DSI) at physiological rates heterosynaptically enhances the strength of output synapses made by another swim interneuron, C2, onto neurons in the pedal ganglion. Using intracellular electrophysiological recording combined with real-time confocal imaging of C2 (loaded with Oregon Green Bapta 1), it was determined that DSI stimulation increases the amplitude of spike-evoked Ca2+ signals in C2 without altering basal Ca2+ signals. This neuromodulatory action was restricted to distal neurites of C2 where synapses with pedal neurons are located. The effect of DSI stimulation on C2 spike-evoked Ca2+ signals resembled DSI heterosynaptic enhancement of C2 synapses in several measures: both decayed within 15 s, both were abolished by the serotonin receptor antagonist, methysergide, and both were independent of DSI's depolarizing actions on C2. A brief puff of serotonin could mimic the enhancement of spike-evoked Ca2+ signals in the distal neurites of C2, but larger puffs or bath-applied serotonin elicited nonphysiological effects. These results suggest that DSI heterosynaptic enhancement of C2 synaptic strength may be mediated by a local enhancement of spike-evoked Ca2+ signals in the distal neurites of C2.

Commissural potentiation of perforant path evoked responses in the dentate gyrus of the rat

The effects of conditioning stimuli applied to the commissural pathway on the perforant path (PP) evoked EPSP and population spike response were examined in urethane anaesthetized rats. Whereas conditioning stimuli applied to the PP resulted in a short-term potentiation of both the EPSP and population spike evoked by a test pulse to the same pathway (homosynaptic potentiation), only the population spike was potentiated when the PP test pulse was preceded by a conditioning volley to the commissural afferent. This form of heterosynaptic potentiation, which occurs in the absence of any significant change in the synaptic currents generated by the perforant path, suggests that alterations in postsynaptic excitability may underly the process of short-term potentiation rather than an augmented transmitter release.