Impact of network activity on the integrative properties of neocortical
pyramidal neurons in vivo.
Alain Destexhe and Denis Paré
Journal of Neurophysiology 81: 1531-1547, 1999
Abstract
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 a ~5-fold 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 around 0.1) in order 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 less than 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
~5-fold 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
greatly enhanced 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 EEG activity, neocortical neurons are
continuously bombarded 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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