Dynamically interacting processes underlie synaptic plasticity in a feedback pathway

Descending feedback is a common feature of sensory systems. Characterizing synaptic plasticity in feedback inputs is essential for delineating the role of feedback in sensory processing. In this study, we demonstrate that multiple interacting processes underlie the dynamics of synaptic potentiation in one such sensory feedback pathway. We use field recording and modeling to investigate the interaction between the transient high-magnitude potentiation (200-300%) elicited during tetanic stimulation of the feedback pathway and the lower magnitude posttetanic potentiation (PTP; ~30%) that slowly decays on cessation of the tetanus. The amplitude of the observed transient potentiation is graded with stimulus frequency. In contrast, the induction of PTP has a stimulus frequency threshold between 1 and 5 Hz, and its amplitude is independent of stimulus frequency. We suggest that the threshold for PTP induction may be linked to a minimum level of sustained potentiation (MSP) during repetitive trains of stimuli. We have developed a novel model that describes the interaction between the transient plasticity observed during train stimulation and the generation of PTP. The model combines a multiplicative, facilitation-depression-type (FD) model that describes the transient plasticity, with an enzymatic network that describes the dynamics of PTP. The model links transient plasticity to PTP through an input term that reflects MSP. The stratum fibrosum-pyramidal cell (StF-PC) synapse investigated in this study is the terminus of a feedback pathway to the electrosensory lateral line lobe (ELL) of a weakly electric gymnotiform fish. Dynamic plasticity at the StF-PC synapse may contribute to the putative role of this feedback pathway as a sensory searchlight.