Inhibitory control of somatic and dendritic sodium spikes in neocortical
pyramidal neurons in vivo: an intracellular and computational study
Denis Paré, Erik Lang and Alain Destexhe
Neuroscience 84: 377-402, 1998
Abstract
The effect of synaptic inputs on somatodendritic interactions during
action potentials was investigated using in vivo intracellular recording and
computational models of neocortical pyramidal cells. An array of 10
microelectrodes, each ending at a different cortical depth, was used to
preferentially evoke synaptic inputs to different somatodendritic regions.
Relative to action potentials evoked by current injection, spikes elicited by
cortical microstimuli were reduced in amplitude and duration, with stimuli
delivered at proximal (somatic) and distal (dendritic) levels evoking the
largest and smallest decrements, respectively. When the IPSP reversal was
shifted to around -50 mV by recording with KCl pipettes, synaptically evoked
spikes were significantly less reduced than with potassium acetate or cesium
acetate pipettes, suggesting that spike decrements are not only due to a
shunt, but also to voltage-dependent effects.
Computational models of neocortical pyramidal cells were built based
on available data on the distribution of active currents and synaptic inputs
in the soma and dendrites. The distribution of synapses activated by
extracellular stimulation was estimated by matching the model to experimental
recordings of EPSP/IPSP sequences evoked at different depths. The model
successfully reproduced the progressive spike amplitude reduction as a
function of stimulation depth, as well as the effects of chloride and cesium.
The model revealed that somatic spikes contain an important contribution from
proximal dendritic sodium currents up to about 100 um and 300 um from the soma
under control and cesium conditions, respectively. Proximal IPSPs can prevent
this dendritic participation thus reducing the spike amplitude at the soma.
The model suggests that the somatic spike amplitude and shape can be used as a
"window" to infer the electrical participation of proximal dendrites. Thus,
our results suggest that IPSPs can control the participation of proximal
dendrites in somatic sodium spikes.
Movies
Several movie files illustrate the dynamics of membrane potential in soma and
dendrites in a simulated neocortical layer V pyramidal neuron. They are an
excellent complement to the figures of the paper. The somatodendritic
distribution of membrane potential is shown by colors in three cases of action
potential generation:
backp_control.mpg Back-propagating action potential following current
injection in the soma
backp_stim_dist.mpg Forward-propagating action potential following
"distal" stimulation
backp_stim_prox.mpg Action potential following stimulation of "proximal"
synapses. In this case, there is no action potential invasion in dendrites
and the amplitude of the somatic spike is reduced (see paper)
See also the book chapter Destexhe A, Lang E and
Paré D. Somato-dendritic interactions underlying action potential
generation in neocortical pyramidal cells in vivo. In: Computational
Neuroscience. Trends in Research (edited by J. Bower), Plenum Press,
New York, pp. 167-172, 1998.
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