Journal of Neuroscience, Vol 10, 2268-2280, Copyright © 1990 by Society for Neuroscience
Voltage-dependent nonlinearities in the membrane of locust nonspiking local interneurons, and their significance for synaptic integration
G Laurent
Department of Zoology, University of Cambridge, England.
Some aspects of the electronic and active membrane properties of nonspiking
local interneurons were studied in isolated locust thoracic ganglia, using
the switched current- and voltage-clamp techniques in neuropilar
recordings. The average transmembrane potential (Vr) of the interneurons
was -58 +/- 6mV (n = 85), and the input resistance (in the linear region of
the current-voltage curve) was 16.5 +/- 8 M omega (n = 19, range 8 to 32 M
omega). The membrane and equalizing time constants were estimated from
charging curves evoked by the injection of low density hyperpolarizing
current pulses from about -80 mV, i.e., from voltages in the linear region
of the I-V curve. The curves yielded 2 time constants (tau m and tau l)
whose average values were 33.2 +/- 9 msec and 3.3 +/- 1 msec (n = 18),
respectively. The mean specific membrane resistance is therefore about 33 k
omega.cm2, assuming that the membrane capacitance is ca. 1 microF.cm-2. An
outward rectification was always observed upon depolarization from
potentials more negative than Vr and was accompanied by a decrease in input
resistance and membrane time constant. The "resting" membrane, for example,
had a time constant of 26.4 +/- 8 msec (n = 31). This outward rectification
was due to at least 2 conductances with different inactivation kinetics,
similar to the transient "A" and "delayed-rectifier" potassium
conductances. No inward rectification was ever observed upon injection of
hyperpolarizing current. In about 60% of the recordings, an active and
TTX-resistant depolarizing process could be evoked by rapid depolarization
around Vr. The voltage-dependent properties of the membrane of the
nonspiking local interneurons had dramatic effects on the shape and time
course of natural or evoked unitary PSPs. The half- width of EPSPs, for
example, decreased by a factor of 7.5 if the membrane potential was shifted
from -93 to -50 mV. When the membrane potential of an interneuron was
altered with a triangular current waveform, the reduction of tonically
occurring IPSPs depended more on the sign and rate of the induced voltage
change than on the absolute transmembrane potential. For 2 identical
instantaneous values of membrane potential, for example, the reduction of
the PSPs was greater during the depolarizing phase than during the
hyperpolarizing phase of the current waveform. The possible nature of the
active membrane conductances underlying the nonlinear electrical behavior
of the membrane is discussed, together with their functional significance
for local circuit synaptic integration.
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