The Journal of Neurophysiology Vol. 78 No. 2 August 1997, pp. 703-720
Copyright ©1997 The American Physiological Society

Comparative Electrotonic Analysis of Three Classes of Rat Hippocampal Neurons

Nicholas T. Carnevale^{1, 2}, Kenneth Y. Tsai^{1, 2}, Brenda J. Claiborne⁴, and Thomas H. Brown^{1, 2, 3}

¹ Center for Theoretical and Applied Neuroscience, ² Department of Psychology, and ³ Department of Cellular and Molecular Physiology, Yale University, New Haven, Connecticut 06520; and ⁴ Division of Life Sciences, University of Texas at San Antonio, San Antonio, Texas 78249

Carnevale, Nicholas T., Kenneth Y. Tsai, Brenda J. Claiborne, and Thomas H. Brown. Comparative electrotonic analysis of three classes of rat hippocampal neurons. J. Neurophysiol. 78: 703-720, 1997. We present a comparative analysis of electrotonus in the three classes of principal neurons in rat hippocampus: pyramidal cells of the CA1 and CA3c fields of the hippocampus proper, and granule cells of the dentate gyrus. This analysis used the electrotonic transform, which combines anatomic and biophysical data to map neuronal anatomy into electrotonic space, where physical distance between points is replaced by the logarithm of voltage attenuation (log A). The transforms were rendered as "neuromorphic figures" by redrawing the cell with branch lengths proportional to log A along each branch. We also used plots of log A versus anatomic distance from the soma; these reveal features that are otherwise less apparent and facilitate comparisons between dendritic fields of different cells. Transforms were always larger for voltage spreading toward the soma (V_in) than away from it (V_out). Most of the electrotonic length in V_out transforms was along proximal large diameter branches where signal loss for somatofugal voltage spread is greatest. In V_in transforms, more of the length was in thin distal branches, indicating a steep voltage gradient for signals propagating toward the soma. All transforms lengthened substantially with increasing frequency. CA1 neurons were electrotonically significantly larger than CA3c neurons. Their V_out transforms displayed one primary apical dendrite, which bifurcated in some cases, whereas CA3c cell transforms exhibited multiple apical branches. In both cell classes, basilar dendrite V_out transforms were small, indicating that somatic potentials reached their distal ends with little attenuation. However, for somatopetal voltage spread, attenuation along the basilar and apical dendrites was comparable, so the V_in transforms of these dendritic fields were nearly equal in extent. Granule cells were physically and electrotonically most compact. Their V_out transforms at 0 Hz were very small, indicating near isopotentiality at DC and low frequencies. These transforms resembled those of the basilar dendrites of CA1 and CA3c pyramidal cells. This raises the possibility of similar functional or computational roles for these dendritic fields. Interpreting the anatomic distribution of thorny excrescences on CA3 pyramidal neurons with this approach indicates that synaptic currents generated by some mossy fiber inputs may be recorded accurately by a somatic patch clamp, providing that strict criteria on their time course are satisfied. Similar accuracy may not be achievable in somatic recordings of Schaffer collateral synapses onto CA1 pyramidal cells in light of the anatomic and biophysical properties of these neurons and the spatial distribution of synapses.

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