Quantitative analyses of anatomical and electrotonic structures of local spiking interneurons by three-dimensional morphometry in crayfish.

We quantitatively investigated the three-dimensional structure of the dendrites of local spiking interneurons using a confocal laser scanning microscope in the terminal abdominal ganglion of crayfish. We also studied their passive membrane properties electrophysiologically using the single-electrode current clamp techniques to analyze their electrotonic structure. All of the local spiking interneurons examined in this study lacked distinctive axonal structure and had a monopolar cell body that was connected with a fine primary process to a thick main segment. Numerous fine secondary processes projected from the main segment in the ganglionic neuropile. The average anatomical length of a secondary process from the main segment to its terminal was 261.9 +/- 15.2 microm. The average input resistance and membrane time constant of local spiking interneurons, obtained from their voltage responses to intracellular injection of step current pulses in the main segment, were 15.2 +/- 1.6 MOmega and 13.9 +/- 1.9 msec, respectively. Calculation of the electrotonic length of dendritic processes based on morphological and physiological data obtained in this study revealed that the average electrotonic length of secondary processes in local spiking interneurons was significantly longer than in local nonspiking interneurons, although both types of local interneurons showed apparently similar anaxonic structure. The steady-state voltage attenuation factors for the secondary processes of local spiking interneurons were significantly greater than those of local nonspiking interneurons in both centrifugal and centripetal directions. The larger electrotonic structure of local spiking interneurons compared to that of nonspiking interneurons appears to be compensated for by their excitable dendritic membrane.

Information processing by nonspiking interneurons: passive and active properties of dendritic membrane determine synaptic integration.

Nonspiking interneurons control activities of postsynaptic cells without generating action potentials in the central nervous system of many invertebrates. Physiological characteristics of their dendritic membrane have been analyzed in previous studies using single electrode current- and voltage-clamp techniques. We constructed a single compartment model of an identified nonspiking interneuron of crayfish. Experimental results allowed us to simulate how the passive and active properties of the dendritic membrane influence the integrative processing of synaptic inputs. The results showed that not only the peak amplitude but also the time course of synaptic potentials were dependent on the membrane potential level at which the synaptic activity was evoked. When the synaptic input came sequentially, each individual input was still discernible at depolarized levels at which the membrane time constant was short due to depolarization-dependent membrane conductances. In contrast, synaptic potentials merged with each other to develop a sustained potential at hyperpolarized levels where the membrane behaved passively. Thus, synaptic integration in a single nonspiking interneuron depends on the value of membrane potential at which it occurs. This probably reflects the temporal resolution required for specific types of information processing.

Quantitative analyses of anatomical and electrotonic structures of crayfish nonspiking interneurons by three-dimensional morphometry.

The three-dimensional structure of premotor nonspiking interneurons in the terminal abdominal ganglion of crayfish have been studied quantitatively by using a confocal laser-scanning microscope. Their passive membrane properties have also been studied electrophysiologically to analyze their electrotonic structure. In either one of the two major morphological types, anterolateral (AL) and posterolateral (PL), that are characterized by different locations of cell bodies in the ganglion, the monopolar cell body is connected with a fine primary process to a thick main segment projecting numerous fine secondary processes. These two types of cells share a common dendritic field in the neuropil, showing similar anatomical characteristics of dendrites. Electrotonic analyses based on the present anatomical and physiological measurements have revealed that the steady-state voltage-attenuation factors for the secondary processes were not statistically different between the AL- and PL-type cells. Comparison between the premotor nonspiking interneurons and an identified sensory nonspiking interneuron, which was studied previously, has revealed that voltage attenuation over secondary processes in both the centripetal and the centrifugal directions was significantly greater in the sensory than in the premotor interneurons, although the anatomical length of each secondary process from its terminal to the main segment was not different between them. Differences in the electrotonic structure between sensory and premotor nonspiking interneurons indicate their different modes of synaptic integration in the control of postsynaptic nerve cells.