Inhibitory control of somatodendritic interactions underlying action potentials in neocortical pyramidal neurons in vivo: An intracellular and computational study

Abstract

Abstract--The effect of synaptic inputs on somatodendritic interactions during action potentials was investigated, in the cat, 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 inhibitory postsynaptic potential 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 postsynaptic potentials 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 ]100 µm and ]300 µm from the soma under control and cesium conditions, respectively. Proximal inhibitory postsynaptic potentials 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 inhibitory postsynaptic potentials can control the participation of proximal dendrites in somatic sodium spikes.1998 IBRO. Published by Elsevier Science Ltd.Key words: multicompartment models, intrinsic electrophysiological properties, in vivo intracellular recordings, action potentials, dendritic integration.By comparing the shape of antidromic, orthodromic and current-evoked action potentials (APs) in motoneurons, Coombs et al. 7 provided compelling evidence for the idea that APs are initiated at the initial segment (IS) and then invade the somatodendritic compartment. However, the applicability of this model to other cell types was questioned when the first intradendritic recordings revealed that dendrites can sustain active electrogenesis. 33,34,63 In neocortical and hippocampal pyramidal neurons for instance, intracellular recordings revealed that dendritic spikes can be elicited by synaptic inputs 5,9,30,52 and that they can amplify synaptic inputs electrotonically distant from the soma to initiate APs. 5 Moreover, the prox...

Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons

“…Other contributions to spike shape might come from the properties of the dendritic tree. An in vivo analysis and a detailed model have shown that dendritic sodium channels contribute to spike shape (Paré et al, 1998). Models using four compartments reproduce this result for the naturalistic stimulation used experimentally and suggest that, at least in the model, this effect is smaller than that of the conductance history (Supplement 3, available at www.jneurosci.org as supplemental material).…”

“…An influence of action potential shape was evident only from differences between pyramidal and Purkinje neurons and from modeling. A possible mechanism for variability in the action potential shape within a neuron is the variable participation of dendritic sodium currents, which can be prevented by proximal IPSPs (Paré et al, 1998). …”

Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons

“…In vivo, the depolarizing effect would be greatest during periods of slow firing and for neurons with large afterhyperpolarizations that go below E rev . If E rev were significantly more negative (e.g., approximately Ϫ75 mV), as has been suggested by some in vivo intracellular studies in adult cortex (Pare et al, 1998), the depolarizing effect would become less significant.…”

Studies of stimulus parameters for seizure disruption using neural network simulations

“…n syn represents the total number of synapses for a given cell-cell connection and is taken from data when possible (Douglas and Martin 1990;Krimer and Goldman-Rakic 2001;Kalisman et al 2003;Kisvárday et al 2002;DeFelipe 1985). R j represents a factor for the relative receptor density, is taken as 1 for excitatory cells, and derived from (Paré et al 1998) for the inhibitory cell types. Table 3 Single neuron simulations using modified Hodgkin-Huxley equations with calcium diffusion.…”