Synaptic mechanisms of a tonic EPSP in crustacean visual interneurons: analysis and simulation

Abstract

Light-evoked synaptic responses of identified visual interneurons, sustaining fibers (SFs), were quantitatively analyzed, and a neuronal cable model was used to calculate voltage attenuations and predict synaptic responses. The cable model is based on morphological measurements of SFs filled with Lucifer yellow and passive membrane properties assessed by current injection in the proximal portion of the dendritic arbor. The morphological and electrophysiological measurements were made in different preparations on homologues of the same identified interneurons. The excitatory postsynaptic potential (EPSP) elicited with high-intensity light consists of a transient phase (mean amplitude 33.1 mV) and a second phase (the plateau) that decays slowly relative to the membrane time constant (mean amplitude 24.4 mV). The mean extrapolated reversal potentials are -19.1 mV for the transient and -22.3 mV during the plateau. The change in input conductance associated with the plateau phase of the response showed a peak of 121% above the resting input conductance and decayed to approximately 50% above resting conductance over several seconds. Compartmental cable models (18, 19) were used to calculate voltage attenuations and local synaptic conductances within the SF dendritic tree. The dendrites are electrotonically compact, and voltage attenuations average 6% for current flowing distally from the recording site (injected) and 45% for current flowing proximally to the recording site. The steady-state EPSP is associated with a calculated 80% decrease in the net dendritic membrane resistivity. The synaptic response, calculated for an EPSP distributed throughout the dentritic tree (using this conductance change and the measured steady-state reversal potential) was 27.0 mV, compared with an observed mean value of 24.4 mV. The calculated relationship between steady-state EPSP amplitude and dendritic membrane resistivity (Rs) is a sigmoidal function that resembles the intensity/response function of the SF. We can therefore correctly predict the transformation from light intensity to compound EPSP amplitude by calculating the intervening synaptic membrane resistivity and voltage values. These functions are affected in a predictable manner by the passive membrane resistivity (Rm) and the EPSP reversal potentials. Tetrodotoxin (TTX) application abolished all SF spiking but left the EPSP essentially unchanged, suggesting that the neuronal pathway from photoreceptors to SFs is mainly or entirely comprised of nonspiking (i.e., TTX-insensitive) elements.