Subthreshold Membrane Resonance in Neocortical Neurons.
Hutcheon, Bruce, Robert M. Miura, and Ernest Puil.
Department of Pharmacology & Therapeutics, Faculty of Medicine, Department
of Mathematics, and Institute of Applied Mathematics, The University of
British Columbia, ancouver, B.C., Canada V6T 1Z3.
APStracts 3:0049N, 1996.
SUMMARY AND CONCLUSIONS
1. Using whole-cell recording techniques, we studied subthreshold and
suprathreshold voltage responses to oscillatory current inputs in neurons from
the sensorimotor cortex of juvenile rats. 2. Based on firing patterns, neurons
were classified as regular spiking (RS), intrinsic bursting (IB), and fast
spiking (FS). The subthreshold voltage-current relationships of RS and IB
neurons were rectifying whereas FS neurons were nearly ohmic near rest. 3.
Frequency response curves (FRCs) for neurons were determined by analyzing the
frequency content of inputs and outputs. The FRCs of most neurons were
voltage-dependent at frequencies below, but not above, 20 Hz. Approximately
60% of RS and IB neurons had a membrane resonance at their resting potential.
Resonant frequencies were between 0.7 and 2.5 Hz (24-26 degrees ? C) near -70
mV and usually increased with hyperpolarization and decreased with
depolarization. The remaining RS and IB neurons and all FS neurons were
nonresonant. 4. Resonant neurons near rest had a selective coupling between
oscillatory inputs and firing. These neurons selectively fired action
potentials when the frequency of the swept-sine-wave (ZAP) current input was
near the resonant frequency. However, when these neurons were depolarized to -
60 ? mV, spike firing was associated with many input frequencies rather than
selectively near the resonant frequency. 5. We examined three subthreshold
currents that could cause low-frequency resonance: I H , a slow,
hyperpolarization-activated cation current that was blocked by external Cs +
but not Ba 2+ ; I IR, , an instantaneously-activating, inwardly-rectifying K +
current that was blocked by both Cs + and Ba 2+ ; and I NaP , an quickly-
activating, inwardly-rectifying persistent Na + current that was blocked by
tetrodotoxin (TTX). Voltage clamp experiments defined the relative steady-
state activation ranges of these currents. I IR (activates below -80 mV) and I
Na,p (activates above -65 mV) are unlikely to interact with each other because
their activation ranges never overlap. However, both currents may interact
with I H which activated variably at potentials between -50 and -90 mV in
different neurons. 6. We found that I H produces subthreshold resonance.
Consistent with this, subthreshold resonance was blocked by external Cs + but
not Ba 2+ or TTX. Application of Ba 2+ enlarged FRCs and resonance at
potentials below -80 mV indicating that I K,ir normally attenuates resonance.
Application of TTX greatly diminished resonance at potentials more depolarized
than -65 mV indicating that I NaP normally amplifies resonance at these
potentials. 7. The ZAP current input may be viewed as a model of oscillatory
currents that arise in neocortical neurons during synchronized activity in the
brain. We propose that the frequency selectivity endowed on neurons by I H may
contribute to their participation in synchronized firing. The voltage
dependence of the frequency-selective coupling between oscillatory inputs and
spikes may indicate a novel mechanism for controlling the extent of low-
frequency synchronized activity in the neocortex.
Received 17 October 1995; accepted in final form 4 March 1996.
APS Manuscript Number J697-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 20 March 96