ELECTROTONIC ARCHITECTURE OF HIPPOCAMPAL CA1 PYRAMIDAL NEURONS BASED ON 3-DIMENSIONAL RECONSTRUCTIONS

1. The spread of electrical signals in pyramidal neurons from the CA1 field of rat hippocampus was investigated through multicompartmental m odeling based on three-dimensional morphometric reconstructions of fou r of these cells. These models were used to dissect the electrotonic a rchitecture of these neurons, and to evaluate the equivalent cylinder approach that this laboratory and others have previously applied to th em. Robustness of results was verified by the use of wide ranges of va lues of specific membrane resistance (R(m)) and cytoplasmic resistivit y. 2. The anatomy exhibited extreme departures from a key assumption o f the equivalent cylinder model, the so-called ''3/2 power law.'' 3. T he compartmental models showed that the frequency distribution of stea dy-state electrotonic distances between the soma and the dendritic ter minations was multimodal, with a large range and a sizeable coefficien t of variation. This violated another central assumption of the equiva lent cylinder model, namely, that all terminations are electrotonicall y equidistant from the soma. This finding, which was observed both for ''centrifugal'' (away from the soma) and ''centripetal'' (toward the soma) spread of electrical signals, indicates that the concept of an e quivalent electrotonic length for the whole dendritic tree is not appr opriate for these neurons. 4. The multiple peaks in the electrotonic d istance distributions, whether for centrifugal or centripetal voltage transfer, were clearly related to the laminar organization of synaptic afferents in the CA1 region. 5. The results in the three preceding pa ragraphs reveal how little of the electrotonic architecture of these n eurons is captured by a simple equivalent cylinder model. The multicom partmental model is more appropriate for exploring synaptic signaling and transient events in CA1 pyramidal neurons. 6. There was significan t attenuation of synaptic potential, current, and charge as they sprea d from the dendritic tree to the soma. Charge suffered the least and v oltage suffered the most attenuation. Attenuation depended weakly on R (m) and strongly on synaptic location. Delay of time to peak was more distorted for voltage than for current and was more affected by R(m). 7. Adequate space clamp is not possible for most of the synapses on th ese cells. Application of a somatic voltage clamp had no significant e ffect on voltage transients in the subsynaptic membrane. 8. The possib le existence of steep voltage gradients within the dendritic tree is c onsistent with the idea that there can be some degree of local process ing and that different regions of the neuron may function semiautonomo usly. These spatial gradients are potentially relevant to synaptic pla sticity in the hippocampus, and they also suggest caution in interpret ing some neurophysiological results.