CHANGES IN SYNAPTIC INTEGRATION DURING THE GROWTH OF THE LATERAL GIANT-NEURON OF CRAYFISH

1. The effect of growth on the electrotonic structure and synaptic int egrative 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 sm all and large LGs were compared with model responses to determine whet her the differences in the neurons' responses result from growth-relat ed changes in their physical characteristics. 2. LG neurons in the ter minal abdominal ganglia of small and large crayfish are similar in sha pe 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 ipsilatera l dendrite of LG in the horizontal plane of the terminal abdominal gan glion is 27 times larger in the large than in the small crayfish. 3. L G'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 crayfis h (8.6 ms). 4. Simultaneous recordings were made from the distal porti on of the ipsilateral dendrite and the initial axon segment of small a nd large LGs to determine how excitatory postsynaptic potentials (EPSP s) are attenuated or filtered by the electrotonic properties of the di fferent sized cells. In the small LG, the fast alpha and the slower be ta components of compound EPSPs evoked by sensory nerve stimulation we re similarly attenuated. In the large LG, the alpha component of the c ompound EPSP was much more attenuated and smoothed than the slower bet a component. 5. Multicompartment models of small and large LGs were co nstructed and used to test whether differences in the two neurons' phy sical properties could account for the differences in their passive re sponse properties. Values for the compartmental resistances, capacitan ces 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 membra ne properties of both cells were uniform, that the specific membrane c apacitance equalled 1 mu F/cm(2), and that the cytoplasmic resistivity equalled 60 Omega-cm. 6. The models were presented with patterns of s imulated synaptic inputs that evoked EPSPs in dendritic compartments t hat were similar to EPSPs recorded in the dendrites of the two cells. The EPSPs spread to the initial axon segment compartments where they w ere similar to EPSPs recorded at the corresponding initial axon segmen ts of the two cells. This result indicates that differences in the pas sive properties of large and small LGs can account for the different w ays they filter EPSPs. 7. Differences in the integrative properties of the two models were assessed by calculating the centripetal attenuati on of DC, 10-, 100-, and 1,000-Hz voltages from a dendritic end compar tment to the initial axon segment compartment. Attenuation in the smal l 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 attenuate d. Reducing the membrane time constant of the large model to the value of the small model reduces DC attenuation to the level obtained in th e small model, but has little effect on the greater attenuation of hig h-frequency signals. 8. We concluded that the growth of LG enhances th e attenuation and low-pass filtering of EPSPs as they conduct passivel y from the dendrites to the initial axon segment. The low-pass filter results from the approximately isometric pattern of neuronal growth an d from the increase in tau(m). Isometric growth increases the attenuat ion of all EPSPs, but affects phasic EPSPs much more than tonic EPSPs. The increase in tau(m) reduces the attenuation of DC and low-frequenc y EPSP components to the levels in the small LG, but has minimal effec ts on the attenuation of phasic components. This change in LG's integr ative properties accounts for the growth-related increase in the atten uation 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.