J Neurophysiol (April 1, 2003). 10.1152/jn.00956.2002
Submitted on Submitted 24 October 2002; accepted in final form 11 December 2002
Effect of Neuritic Cables on Conductance Estimates for Remote
Electrical Synapses
Astrid A.
Prinz and
Peter
Fromherz
Department of Membrane and Neurophysics, Max Planck Institute for
Biochemistry, D 82152 Martinsried, Germany
Prinz, Astrid A. and
Peter Fromherz.
Effect of Neuritic Cables on Conductance Estimates for Remote
Electrical Synapses. J. Neurophysiol. 89: 2215-2224, 2003. The conductance of electrical
synapses is usually estimated from voltage recordings at the neuronal
somata under the assumption that each cell is isopotential. This
approach neglects effects of intervening neurites. For a cell pair with
unbranched neurites and an electrical synapse at their ends, we used
cable theory to derive an analytical expression that relates the
synaptic conductance to voltage recordings at the cell bodies and to
the neurite properties. The equation implies that the conventional
method significantly underestimates the actual synapse conductance if
the neurite length is comparable to the electrotonic length constant
and if the synaptic conductance is similar to the serial neurite
conductance. For an experimental test, we cultured pairs of snail
neurons on protein patterns, resulting in a geometry that matched the
theoretical model. Using the isopotential theory, we estimated the
synapse conductances and found them to be rather weak. To obtain the
cable properties, we recorded spatiotemporal maps of signal propagation in the neurites using a voltage-sensitive dye. Fits of these maps to a
passive cable model showed that the snail neurons are electrotonically rather compact. Given these features of our experimental system, the
synaptic conductances derived with the nonisopotential model deviated
from the estimates of the isopotential theory by about 13%. This
discrepancy, although small, shows that even in electrotonically compact neurons coupled by weak synapses the impact of the neuritic cables on conductance estimates cannot be neglected. When applied to
less compact and more strongly coupled cell pairs in vivo, our approach
can supply the realistic estimates of synaptic conductances that are
necessary for a better understanding of the role of electrical coupling
in neural systems.