1. The effect of growth on the electrotonic structure and synaptic integrative properties of the lateral giant (LG) interneuron was assessed from anatomic and electrophysiological measurements of LGs in small (1-2.4 cm) and large (9-11.2 cm) crayfish and from calculated responses of mathematical models of these neurons. Postsynaptic responses of small and large LGs were compared with model responses to determine whether the differences in the neurons' responses result from growth-related changes in their physical characteristics. 2. LG neurons in the terminal abdominal ganglia of small and large crayfish are similar in shape but differ in size according to an approximately isometric pattern of growth. The soma diameter of the large LG is 2.2 times larger than the small LG, the major ipsilateral dendrite is 2.8 times longer and 3.6 times greater in diameter, and the axon is 7.6 times longer and 4.5 times greater in diameter. The projected area of the major ipsilateral dendrite of LG in the horizontal plane of the terminal abdominal ganglion is 27 times larger in the large than in the small crayfish. 3. LG's input resistance was nearly 80% smaller in the large (167 K Omega) than in the small (742 K Omega) crayfish when measured at or near the initial axon segment. The cell's membrane time constant displayed an opposite relationship, with the value in the large crayfish (20.9 ms) nearly two-and-a-half times larger than the value in the small crayfish (8.6 ms). 4. Simultaneous recordings were made from the distal portion of the ipsilateral dendrite and the initial axon segment of small and large LGs to determine how excitatory postsynaptic potentials (EPSPs) are attenuated or filtered by the electrotonic properties of the different sized cells. In the small LG, the fast alpha and the slower beta components of compound EPSPs evoked by sensory nerve stimulation were similarly attenuated. In the large LG, the alpha component of the compound EPSP was much more attenuated and smoothed than the slower beta component. 5. Multicompartment models of small and large LGs were constructed and used to test whether differences in the two neurons' physical properties could account for the differences in their passive response properties. Values for the compartmental resistances, capacitances and coupling resistances were determined from measurements of the lengths and diameters of the neuronal processes and from the measured membrane time constants, under the assumptions that the passive membrane properties of both cells were uniform, that the specific membrane capacitance equalled 1 mu F/cm(2), and that the cytoplasmic resistivity equalled 60 Omega-cm. 6. The models were presented with patterns of simulated synaptic inputs that evoked EPSPs in dendritic compartments that were similar to EPSPs recorded in the dendrites of the two cells. The EPSPs spread to the initial axon segment compartments where they were similar to EPSPs recorded at the corresponding initial axon segments of the two cells. This result indicates that differences in the passive properties of large and small LGs can account for the different ways they filter EPSPs. 7. Differences in the integrative properties of the two models were assessed by calculating the centripetal attenuation of DC, 10-, 100-, and 1,000-Hz voltages from a dendritic end compartment to the initial axon segment compartment. Attenuation in the small LG is nearly constant from DC to 100 Hz and only increases above 100 Hz. DC potentials in the large LG experience the same attenuation as in the small LG, but signals from below 100 Hz are much more attenuated. Reducing the membrane time constant of the large model to the value of the small model reduces DC attenuation to the level obtained in the small model, but has little effect on the greater attenuation of high-frequency signals. 8. We concluded that the growth of LG enhances the attenuation and low-pass filtering of EPSPs as they conduct passively from the dendrites to the initial axon segment. The low-pass filter results from the approximately isometric pattern of neuronal growth and from the increase in tau(m). Isometric growth increases the attenuation of all EPSPs, but affects phasic EPSPs much more than tonic EPSPs. The increase in tau(m) reduces the attenuation of DC and low-frequency EPSP components to the levels in the small LG, but has minimal effects on the attenuation of phasic components. This change in LG's integrative properties accounts for the growth-related increase in the attenuation of the phasic alpha EPSP relative to the slower beta EPSP, and thereby accounts for the onset of habituation of the crayfish tailflip escape response.
