Nanoconnectomic upper bound on the variability of synaptic plasticity

  1. Thomas M Bartol Jr  Is a corresponding author
  2. Cailey Bromer
  3. Justin Kinney
  4. Michael A Chirillo
  5. Jennifer N Bourne
  6. Kristen M Harris  Is a corresponding author
  7. Terrence J Sejnowski  Is a corresponding author
  1. Howard Hughes Medical Institute, Salk Institute for Biological Studies, United States
  2. Massachusetts Institute of Technology, United States
  3. The University of Texas at Austin, United States
  4. University of California, San Diego, United States
8 figures and 1 table

Figures

Figure 1 with 1 supplement
Correlations among metrics of dendritic spine morphology.

Strong correlations were found between (A) Spine head area and spine head volume, (B) PSD area and spine head volume, and (C) Spine head area and PSD area. (D) Weak correlation was found between …

https://doi.org/10.7554/eLife.10778.003
Figure 1—figure supplement 1
Area of postsynaptic density plotted against spine head volume.

Nine individual dendrites all have similar slopes that are not significantly different showing the uniformity of this comparison across dendrites. Error bars, regression lines and equations as …

https://doi.org/10.7554/eLife.10778.004
Presynaptic docked vesicle numbers are correlated with PSD areas, spine head volumes, and neck diameter, but not with neck length.

(A) All 31,377 presynaptic vesicles. (B) En face view of the 24 docked vesicles (gray spheres) viewed through an axon (green) onto the PSD (red) of example spine (yellow). (C) Number of docked …

https://doi.org/10.7554/eLife.10778.005
Figure 3 with 1 supplement
Morphometric analysis of 287 complete spines in reconstruction.

Distributions of (A) spine head volumes, (B) PSD areas, (C) docked vesicles, (D) spine neck volumes, (E) spine neck diameters, and (F) spine neck lengths are highly skewed with a long tail.

https://doi.org/10.7554/eLife.10778.006
Figure 3—figure supplement 1
Spine measurement and estimation of measurement error.

(A) Example segmentation of spine head (yellow), neck (gray), and PSD area (red). (B) Histogram of the measurement error across all spines measured. (C) Measurement error plotted against spine head …

https://doi.org/10.7554/eLife.10778.007
Figure 4 with 4 supplements
Spine head volumes, PSD areas and neck diameters, but not neck lengths, are highly correlated between pairs of axon-coupled same-dendrite spines.

(A) Visualization of a pair of spines (gray necks) from the same dendrite (yellow) with synapses (red, indicated by white arrows) on the same axon (black stippling) with presynaptic vesicles (white …

https://doi.org/10.7554/eLife.10778.008
Figure 4—figure supplement 1
Analysis of whole spine volume and spine neck volume of axon-coupled same dendrite spines.

(A) Whole spine volumes of pairs of axon-coupled spines on the same dendrite are highly correlated and significantly different from random pairs (KS test p = 0.018). (B) Correlation of neck volumes …

https://doi.org/10.7554/eLife.10778.009
Figure 4—figure supplement 2
Analysis of spines paired randomly.

Distributions represent random pairings of (A) spine head volumes, (B) PSD areas, (C) docked vesicles, (D) neck volumes, (E) neck diameters, and (F) neck lengths, from the population of complete …

https://doi.org/10.7554/eLife.10778.010
Figure 4—figure supplement 3
Axon-coupled same dendrite pairs a–f.

Large white arrows indicate the red PSDs of the spine pairs, the edited necks are dark gray, and the axons are stippled black with vesicles inside. These illustrate how the axon weaves through the …

https://doi.org/10.7554/eLife.10778.011
Figure 4—figure supplement 4
Axon-coupled same-dendrite pairs g-m, illustrated in same way as in Figure 4—figure supplement 3.
https://doi.org/10.7554/eLife.10778.012
CV of axon-coupled spines on the same dendrite does not vary with spine size.

There is no significant correlation, which implies that paired small synapses are as precisely matched as paired large synapses.

https://doi.org/10.7554/eLife.10778.013
Figure 6 with 2 supplements
Paired spine head volumes are not correlated when they are not both axon and dendrite coupled.

(A) Representative visualization and (B) plot showing lack of correlation between spine head volumes of all pairs of axon-coupled spines on different dendrites (n=127). (C) Similarly, randomly …

https://doi.org/10.7554/eLife.10778.014
Figure 6—figure supplement 1
Morphologies of PSD, docked vesicles, and necks are not correlated when spines are not both axon and dendrite coupled.

There is no correlation between (A) PSD areas, (B) docked vesicles, (C) neck diameters, and (D) neck lengths, in pairs of axon-coupled spines on different dendrites.

https://doi.org/10.7554/eLife.10778.015
Figure 6—figure supplement 2
Difference in volume between pairs of axon-coupled spines exhibits a weak trend with separation distance.

Differences in spine head volumes plotted against: A) Distance along the axon for axon-coupled spines on the same dendrite; B) Distance along the axon for axon-coupled spines on different dendrites; …

https://doi.org/10.7554/eLife.10778.016
Proximity of the glial cell to axon-coupled dendritic spines on either the same or different dendrites.

Proximity of astrocytic glial processes is not significantly correlated with spine head volumes of axon coupled pairs. (A) Histogram of spine head volume for spines that contain a spinule that is …

https://doi.org/10.7554/eLife.10778.017
Distinguishable spine sizes.

Over the factor of 60 range in spine head volumes from the data set there are 26 distinguishable intervals of spine sizes with a discrimination probability of 69% for each interval based on signal …

https://doi.org/10.7554/eLife.10778.018

Tables

Table 1

Lower bounds on time window for averaging binomially distributed synaptic input to achieve CV = 0.083.

https://doi.org/10.7554/eLife.10778.019
Release probability
(pr)
Presynaptic spikes
(n)
Averaging time
(R = 1 Hz)
Averaging time
(R = 25 Hz)
0.1130621.8 min52.2 sec
0.25819.68 min23.2 sec
0.51452.42 min5.8 sec

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