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The Journal of Neurophysiology Vol. 81 No. 4 April 1999, pp. 1531-1547
Copyright ©1999 by the American Physiological Society
Laboratoire de Neurophysiologie, Département de Physiologie, Université Laval, Quebec G1K 7P4, Canada
Destexhe, Alain and
Denis Paré.
Impact of network activity on the integrative properties of neocortical
pyramidal neurons in vivo. During wakefulness, neocortical neurons are subjected to an intense synaptic bombardment. To assess the
consequences of this background activity for the integrative properties
of pyramidal neurons, we constrained biophysical models with in vivo
intracellular data obtained in anesthetized cats during periods of
intense network activity similar to that observed in the waking state.
In pyramidal cells of the parietal cortex (area 5-7), synaptic
activity was responsible for an approximately fivefold decrease in
input resistance (Rin), a more depolarized membrane potential (Vm), and a marked increase
in the amplitude of Vm fluctuations, as
determined by comparing the same cells before and after microperfusion
of tetrodotoxin (TTX). The model was constrained by measurements of
Rin, by the average value and standard deviation
of the Vm measured from epochs of intense
synaptic activity recorded with KAc or KCl-filled pipettes as well as
the values measured in the same cells after TTX. To reproduce all experimental results, the simulated synaptic activity had to be of
relatively high frequency (1-5 Hz) at excitatory and inhibitory synapses. In addition, synaptic inputs had to be significantly correlated (correlation coefficient ~0.1) to reproduce the amplitude of Vm fluctuations recorded experimentally. The
presence of voltage-dependent K+ currents, estimated from
current-voltage relations after TTX, affected these parameters by
<10%. The model predicts that the conductance due to synaptic
activity is 7-30 times larger than the somatic leak conductance to be
consistent with the approximately fivefold change in
Rin. The impact of this massive increase in conductance on dendritic attenuation was investigated for passive neurons and neurons with voltage-dependent
Na+/K+ currents in soma and dendrites. In
passive neurons, correlated synaptic bombardment had a major influence
on dendritic attenuation. The electrotonic attenuation of simulated
synaptic inputs was enhanced greatly in the presence of synaptic
bombardment, with distal synapses having minimal effects at the soma.
Similarly, in the presence of dendritic voltage-dependent currents, the
convergence of hundreds of synaptic inputs was required to evoke action
potentials reliably. In this case, however, dendritic voltage-dependent
currents minimized the variability due to input location, with distal
apical synapses being as effective as synapses on basal dendrites. In conclusion, this combination of intracellular and computational data
suggests that, during low-amplitude fast electroencephalographic activity, neocortical neurons are bombarded continuously by correlated synaptic inputs at high frequency, which significantly affect their
integrative properties. A series of predictions are suggested to test
this model.
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