Functional Significance of Passive and Active Dendritic Properties in the Synaptic Integration by an Identified Nonspiking Interneuron of Crayfish

Abstract

Nonspiking interneurons control their synaptic output directly by membrane potential changes caused by synaptic activities. Although these interneurons do not generate spikes, their dendritic membrane is endowed with a variety of voltage-dependent conductances whose functional significance in synaptic integration remains unknown. We quantitatively investigated how the passive and active dendritic properties affect the synaptic integration in an identified nonspiking interneuron of crayfish by computer simulation using its multicompartment model based on electrophysiological measurements and three-dimensional morphometry. At the resting potential level, the attenuation factor (V(s)/V(t)) of a unitary synaptic potential in the course of its spread from a dendritic terminal (V(s)) to other terminals (V(t)) ranged from 4.42 to 6.30 with no substantial difference between hyperpolarizing and depolarizing potentials. The compound synaptic responses to strong mechanosensory stimulation could be reproduced in calculation only as the result of spatial summation of attenuated potentials, not as any single large potential. The characteristic response could be reproduced by assuming that the active conductances were distributed only in the dendritic region where the synaptic summation was carried out. The active conductances in other parts of the cell affected neither the shape of the compound synaptic response nor the dendritic spread of synaptic potentials. These findings suggest that the active membrane conductances do not affect the spatial distribution of synaptic potentials over dendrites but function in sculpting the summed synaptic potential to enhance temporal resolution in the synaptic output of the nonspiking interneuron.