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bioRxiv · 10.1101/2022.02.15.480607

Contribution of individual excitatory synapses on dendritic spines to electrical signaling

Abstract

Dendritic spines, small ([~]1 {micro}m) membrane protrusions from neuronal dendrites which receive most of the excitatory synaptic inputs in the mammalian brain, are widely considered the elementary computational units of the brain. Our understanding of electrical signalling in spines is currently being debated, primarily for methodological reasons. We combined the standard techniques of whole-cell recording and voltage imaging methods to study excitatory postsynaptic potentials evoked by two-photon glutamate uncaging (uEPSPs) on individual dendritic spines on basal dendrites in rat cortical slices. We analyzed the initiation, temporal summation, and propagation of uEPSPs from the spine head to the parent dendrites in three principal neocortical pyramidal neuron classes. Our measurements show no significant attenuation of uEPSPs across the spine neck in most tested mushroom spines on basal dendrites. This result implies that spine synapses are not electrically isolated from parent dendrites and that these spines do not serve a meaningful electrical role. Using the same high-sensitivity voltage imaging techniques, we characterized the temporal summation of uEPSPs induced by repetitive glutamate uncaging mimicking burst activity of presynaptic neurons. We found that responses to high-frequency repetitive quantal EPSPs are strictly limited in amplitude and waveform. This finding reveals a biophysical mechanism for preventing synaptic saturation. Significance StatementWe used an electrochromic voltage-sensitive dye, which acts as a transmembrane optical voltmeter, to define the electrical role of dendritic spines, small membrane protrusions that receive most of the excitatory synaptic inputs in the brain. The data argue that investigated spine synapses of principal neurons are not electrically isolated from the parent dendrites. We also found that the amplitude of temporal uEPSP summation during repetitive synaptic activation is restricted at the site of origin, preventing synaptic saturation. These results facilitate our understanding of how a complex assembly of receptors and ion channels in spines generates and processes electrical signals and mediate plasticity in response to the quantal release of chemical transmitters caused by patterned activity in presynaptic axons.

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BibTeXRIS

Weng, J.-Y., Ceballos, C., Zecevic, D.. 2022-02-17. Contribution of individual excitatory synapses on dendritic spines to electrical signaling. https://doi.org/10.1101/2022.02.15.480607

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