Geometry and the organizational principle of spine synapses along a dendrite

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Precise information on synapse organization in a dendrite is crucial to understanding the mechanisms underlying voltage integration and the variability in the strength of synaptic inputs across dendrites of different complex morphologies. Here, we used focused ion beam/scanning electron microscope (FIB/SEM) to image the dendritic spines of mice in the hippocampal CA1 region, CA3 region, somatosensory cortex, striatum, and cerebellum (CB). Our results show that the spine geometry and dimensions differ across neuronal cell types. Despite this difference, dendritic spines were organized in an orchestrated manner such that the postsynaptic density (PSD) area per unit length of dendrite scaled positively with the dendritic diameter in CA1 proximal stratum radiatum (PSR), cortex and CB. The ratio of the PSD area to neck length was kept relatively uniform across dendrites of different diameters in CA1 PSR. Computer simulation suggests that a similar level of synaptic strength across different dendrites in CA1 PSR enables the effective transfer of synaptic inputs from the dendrites towards soma. Excitatory postsynaptic potentials (EPSPs), evoked at single spines by glutamate uncaging and recorded at the soma, show that the neck length is more influential than head width in regulating the EPSP magnitude at the soma. Our study describes thorough morphological features and the organizational principles of dendritic spines in different brain regions.

Significance statement Little is known about the characteristic anatomical features underlying the organization of spine synapses in a dendrite. This study used volume electron microscopy to make an extensive characterization of dendritic spine synapses in multiple regions of the mouse brain to uncover the principles underlying their placement along a dendritic shaft. By using a combination of approaches such as two-photon imaging, glutamate uncaging, electrophysiology, and computer simulation, we reveal the functional importance of regulated spine placement along a dendritic trunk. Our research presents a crucial step in understanding the synaptic computational principle in dendrites by highlighting the generalizable features of dendritic spine organization in a neuron.

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