Dendritic Excitability and Neuronal Morphology as Determinants of Synaptic Efficacy

Abstract

Komendantov AO, Ascoli GA. Dendritic excitability and neuronal morphology as determinants of synaptic efficacy. J Neurophysiol 101: 1847-1866, 2009. First published January 28, 2009 doi:10.1152/jn.01235.2007. The ability to trigger neuronal spiking activity is one of the most important functional characteristics of synaptic inputs and can be quantified as a measure of synaptic efficacy (SE). Using model neurons with both highly simplified and real morphological structures (from a single cylindrical dendrite to a hippocampal granule cell, CA1 pyramidal cell, spinal motoneuron, and retinal ganglion neurons) we found that SE of excitatory inputs decreases with the distance from the soma and active nonlinear properties of the dendrites can counterbalance this global effect of attenuation. This phenomenon is frequency dependent, with a more prominent gain in SE observed at lower levels of background inputoutput neuronal activity. In contrast, there are no significant differences in SE between passive and active dendrites under higher frequencies of background activity. The influence of the nonuniform distribution of active properties on SE is also more prominent at lower background frequencies. In models with real morphologies, the effect of active dendritic conductances becomes more dramatic and inverts the SE relationship between distal and proximal locations. In active dendrites, distal synapses have higher efficacy than that of proximal ones because of arising dendritic spiking in thin branches with high-input resistance. Lower levels of dendritic excitability can make SE independent of the distance from the soma. Although increasing dendritic excitability may boost SE of distal synapses in real neurons, it may actually reduce overall SE. The results are robust with respect to morphological variation and biophysical properties of the model neurons. The model of CA1 pyramidal cell with realistic distributions of dendritic conductances demonstrated important roles of hyperpolarization-activated (h-) current and A-type K ϩ current in controlling the efficacy of single synaptic inputs and overall SE differently in basal and apical dendrites. I N T R O D U C T I O NDendrites play a central role in neuronal information processing. Electrical signals from other neurons are transmitted onto dendrites via synaptic inputs, which are located throughout the dendritic tree. The most important functional characteristic of synaptic inputs is their ability to influence neuronal spiking activity. At a strong excitatory synapse, a single action potential (AP) in the presynaptic cell might trigger an AP in the postsynaptic neuron, whereas at a weak excitatory synapse only a subthreshold excitatory postsynaptic potential (EPSP) would be initiated under the same stimulating conditions. In real neuronal networks an individual neuron receives many synaptic inputs from numerous other neurons. Under the appropriate circumstance of background activity, even an individual weak synaptic input can be the determining factor for AP initiation...

In Vivo Dynamic Clamp Study of Ih in the Mouse Inferior Colliculus

“…E: tone stimulus. and on the levels and timing of synaptic activity (Komendantov and Ascoli 2009;Migliore et al 2004;Poolos et al 2002;Santoro and Baram 2003). The amplitude of responses to tones decreased in the presence of I h .…”

The Effect of Cervical Spine Manipulation on Postural Sway in Patients With Nonspecific Neck Pain

“…Synaptic efficacy reflects the ability of an individual synaptic input to evoke somatic postsynaptic potentials sufficient to trigger, or alter spiking activity (Komendantov & Ascoli, 2009). Even simple forms of synaptic regulation can have a profound effect on neural function.…”

Analysis of morphological features of thalamocortical neurons from the ventroposterolateral nucleus of the cat

“…It has been shown that with the same active and passive properties of the dendritic tree, the geometrical (e.g., area) and topological (e.g., partition symmetry) properties strongly influence the neuronal firing patterns and modify the efficacy of back-propagating action potentials or forward propagation of postsynaptic potentials (Duijnhouwer et al, 2001;Sterratt and van Ooyen, 2002;Chklovskii, 2004;van Pelt and Schierwagen, 2004;Gulledge et al, 2005;Timofeeva et al, 2008;Weaver and Wearne, 2008;Katz et al, 2009;Komendantov and Ascoli, 2009).…”