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Calcium transient prevalence across the dendritic arbour predicts place field properties

Abstract

Establishing the hippocampal cellular ensemble that represents an animal’s environment involves the emergence and disappearance of place fields in specific CA1 pyramidal neurons1,2,3,4, and the acquisition of different spatial firing properties across the active population5. While such firing flexibility and diversity have been linked to spatial memory, attention and task performance6,7, the cellular and network origin of these place cell features is unknown. Basic integrate-and-fire models of place firing propose that such features result solely from varying inputs to place cells8,9, but recent studies3,10 suggest instead that place cells themselves may play an active role through regenerative dendritic events. However, owing to the difficulty of performing functional recordings from place cell dendrites, no direct evidence of regenerative dendritic events exists, leaving any possible connection to place coding unknown. Using multi-plane two-photon calcium imaging of CA1 place cell somata, axons and dendrites in mice navigating a virtual environment, here we show that regenerative dendritic events do exist in place cells of behaving mice, and, surprisingly, their prevalence throughout the arbour is highly spatiotemporally variable. Furthermore, we show that the prevalence of such events predicts the spatial precision and persistence or disappearance of place fields. This suggests that the dynamics of spiking throughout the dendritic arbour may play a key role in forming the hippocampal representation of space.

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Figure 1: Co-acquired time-series of CA1 place cell somata, dendrites and axons during virtual navigation.
Figure 2: Variability of dendritic branch spiking during somatic place field firing.
Figure 3: Place field branch-spiking heterogeneity.
Figure 4: Dendritic BSP predicts place field spatial precision and long-term stability.

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Acknowledgements

We are grateful to B. Mensh for discussions on data conceptualization, interpretation and presentation. We thank C. Harvey, B. Mensh, N. Spruston, C. Woolley, W. Kath and L. Looger for comments on the manuscript, E. Han and P. Boueri for technical assistance, and V. Jayaraman, R. Kerr, D. Kim, L. Looger, K. Svoboda from the GENIE Project (Janelia Farm, Howard Hughes Medical Institute) for GCaMP6. This work was supported by The Klingenstein Foundation, The Whitehall Foundation, The Chicago Biomedical Consortium with support from the Searle Funds at The Chicago Community Trust, Northwestern University, The National Institutes of Health (1R01MH101297), and M.S. is an Ellison Medical Foundation Fellow of the Life Sciences Research Foundation.

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Authors

Contributions

M.S. performed the experiments, D.D. built the experimental apparatus, M.S. performed data analysis with strategy suggestions from D.D. Both authors conceived and designed the experiments, interpreted the data and wrote the paper.

Corresponding author

Correspondence to Daniel A. Dombeck.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Somatic and dendritic place field Ca2+-transient amplitudes and onset times.

ac, Histograms of somatic transient peak ΔF/F (a), branch-spike peak ΔF/F (b) and ratio of branch-spike peak ΔF/F to somatic transient peak ΔF/F (c). Inset in a shows the smallest significant amplitudes of somatic transients detected (grey) and their mean (blue; average triggered when grey transients were first >2 s.d. above the baseline). These small transients are nearly identical in amplitude, shape and duration to what is expected from single somatic action potentials based on previous in vivo combined cell-attached and imaging measurements in the visual cortex using GCaMP6f (ref. 21). d, Histogram showing the distribution of branch-spike onset time relative to somatic firing onset. Note that branch-spike onset leading somatic firing onset was not observed, and when branch spiking occurred in multiple branches, their onsets were nearly always simultaneous with respect to each other. Mean ± s.d. is shown for ad. Source data

Extended Data Figure 2 Identifying putative dspikes and discriminating between regenerative and non-regenerative dendritic events.

a, Mean ΔF/F of significant calcium transients localized to a single branch (using the same imaging parameters to measure co-occurring somatic firing and branch spikes in Figs 12, 3, 4), plotted against the area of significant ΔF/F increase (>3 s.d.). The mean ΔF/F and the area of significant fluorescence change was calculated for each transient as follows. ΔF/F movies were generated where each pixel value in each frame of the movie represents the change in fluorescence with respect to the baseline mean for that pixel. The frames during the transient of interest were averaged together and the number of pixels with ΔF/F > 3 were counted, converted to µm2 and used as the area of significant fluorescence change. The mean ΔF/F value for the transient was then calculated as the mean value of the pixels with ΔF/F > 3. Black circles represent known single-spine calcium transients acquired using low resolution time-series acquisition (the same resolution used to identify branch spiking), but confirmed as spines using higher-resolution time-series acquisitions where calcium transients were restricted to the spine head (see d and e). Green circles represent calcium transients restricted to a single dendritic branch and occurring in the absence of somatic firing. Because no high-resolution time-series were acquired from these structures, it was unknown whether they represent transients restricted to single spines or branch spiking. The panels and analysis presented in b and c indicate that a majority of these events are due to branch spiking and not single-spine transients. b, As a combined metric of mean ΔF/F and area of fluorescence change, we normalized mean ΔF/F and area of fluorescence to their maximums and measured the distance from the origin (the normalized Euclidean distance of each point in a); we refer to this metric as the activity area index (AAI). Histogram showing that known spine transients all fall into the lowest AAI bins (black bars; AAI < 40), and most unclassified events (putative dspikes) in a have higher AAIs (green bars). The events in the larger AAI bins (with greater mean ΔF/F covering a larger area; AAI > 40; separated from the lower AAI bins by the dashed line) fit known characteristics of dspikes. c, Using the AAI threshold defined in b, most of the unclassified transients fall into a separate group (red) from the known single-spine calcium transients (8 of the 13 unclassified transients had distinctly larger AAIs compared to spine transients, blue) and were therefore considered branch spikes (putative dspikes). d, Example calcium transients restricted to a single spine head (bottom left) and invading both spine head and shaft (bottom right) in a place cell. Mean somatic place field is indicated by the grey dashed line. e, Example of a stretch of dendrite imaged at low (left) and high (right) resolution in a navigating mouse. The red box and ROIs indicate the same structures that were imaged at both low and high resolution. The same spine head is indicated by arrows at different resolutions in all images. Calcium transients restricted to the same single spine head are shown at both low and high resolution by the colour-coded per cent ΔF/F map and by the per cent ΔF/F traces labelled non-regenerative; note that the shaft ROI includes other non-active spines. Calcium transients invading the branch and all spines are shown at both low and high resolution by the colour-coded per cent ΔF/F map and by the per cent ΔF/F traces at the bottom, labelled regenerative. f, Image of a dendritic branch split into four ROIs. Calcium transients are seen in all parts of the branch during large area branch spiking (see both colour-coded map and traces of per cent ΔF/F). A putative dspike, during navigation, in the same branch causes a significant increase in fluorescence in only part of the branch (ROI 2), which includes the shaft. Source data

Extended Data Figure 3 Expanded views of traces showing the variability in detectable events in the soma, dendrites and axon.

Traces from Fig. 1b showing variable branch-spike prevalence in the same cell. Three events are shown amplified (for the amplified traces, the bottom y-axis scale bar refers to the green, blue and cyan dendritic traces, and the top scale bar refers to the red and brown soma and axon traces).

Extended Data Figure 4 Expanded views of traces showing variability of dendritic branch spiking during somatic place field firing.

a, Traces from Fig. 2 are shown here amplified (each trace has a y-axis scale bar representing 100% ΔF/F). b, Two examples of branch spikes detected in single branches in the absence of detectable somatic firing and branch spiking in other dendrites. In each case the soma y axis is amplified relative to the dendrite traces to show the absence of detectable somatic transients.

Extended Data Figure 5 Branch spiking in a single dendritic plane is representative of activity throughout a large portion of the dendritic arbour and average branch-spike prevalence is independent of the number of sampled branches in the field, their distance from the soma and the resting fluorescence level of the soma.

a, An example of spiking throughout all imaged branches during 3-plane imaging. Co-acquired somatic and dendritic time-series were recorded using three planes; dendritic plane 1 is approximately mid distance between the soma and dendrite tips, dendritic plane 2 is near the branch tips. Numbered arrows indicate branches connected to the imaged soma with the same numbers in dendritic plane 1 and 2 indicating the same branch. An example run through the cell’s somatic place field (grey) and corresponding ΔF/F traces from the soma and numbered branches from the two dendritic planes is shown. Distance along dendrite between branch and soma, and per cent distance from soma to dendritic tip, are on the right of each trace. b, Same as a, except a different cell where branch spiking is absent throughout all imaged branches in both dendritic planes. c, Scatter plot showing the average branch-spike prevalence for individual branches during somatic firing as a function of branch distance from the soma (each point represents one branch). The average branch-spike prevalence for individual branches is not significantly related to the distance from the soma (Spearman’s rank correlation coefficient: P = 0.16; ρ = −0.128). d, Branch-spike peaks normalized to co-occurring somatic peaks during place field traversals from all place cells and branches plotted against branch distance from soma. Spearman’s rank correlation coefficient shows a significant correlation (P = 5.4 × 10−12, ρ = 0.135) and a linear fit shows a significant positive slope within 95% confidence bounds. e, Histogram showing the branch-spike prevalence for individual dendritic branches taken from all cells. f, Average branch-spike prevalence (for each place field) plotted against the number of branches sampled in the imaging field shows no significant correlation (Spearman’s rank correlation coefficient: P = 0.75; ρ = −0.057). g, Average branch-spike prevalence (for each place field) plotted against normalized resting fluorescence intensity of the soma. Relative resting fluorescence between cells was calculated by dividing the mean measured fluorescence of each soma (not during transients; excluding nucleus) by the squared laser power arriving at the soma (which was estimated based on the soma depth below the surface48). Spearman’s rank correlation coefficient shows no significant correlation (P = 0.9, ρ = −0.034). Source data

Extended Data Figure 6 Place field branch spikes in basal and proximal apical dendrites often co-occur.

Co-acquired somatic, basal dendritic and apical dendritic (depicted in cartoon in the centre) time-series from two example place cells showing somatic spiking with co-occurring branch spikes (top) and somatic spiking in the absence of detectable branch spikes (bottom) in the basal and main apical dendrites (89.6 ± 19.5% correlation between spiking in the basals and main apical; mean distance of apical site to soma, 109 ± 38 µm; n = 6 place fields; mean ± s.d.) during place field traversals (grey). Note that our findings from the basal and proximal apical dendrites may not extend to the oblique dendrites or apical tuft.

Extended Data Figure 7 The distribution of branch-spike prevalence differs from a model in which each branch fires independently with a specific probability during place field traversals.

Seven histograms from seven example place fields showing the distribution of branch-spike prevalence in each field for real data (grey bars) and modelled data (red bars). The modelled data was generated for each place field example as follows. The probability (Pi ) that each dendritic branch (i) in the imaging field would spike in the place field was defined as the branch-spike prevalence for the individual branch (total number of traversals in which branch i spiked divided by the total number of traversals; from real data). For modelled/mock place field traversals, each branch fired with its random probability Pi and the branch-spike prevalence (fraction of the total number of branches with spikes during the traversal) was calculated. The distribution of branch-spike prevalence was generated for 1,000 modelled/mock place field traversals (red bars). A two-sample Kolmogorov–Smirnov test was used to compare real and modelled distributions (P values shown in each plot).

Extended Data Figure 8 Average branch-spike prevalence can differ between different place fields of the same cell and also between in-place field and out-of-place field somatic firing.

a, Coloured plots (left) show occurrence of detectable spiking in each branch (blue or black) during somatic place field firing (red) in different co-occurring place fields (A and B, in different running directions) of the same place cell. Right, histograms of branch-spike prevalence on each traversal for the two place fields. Cartoons (far right) do not represent real data. Note that the running behaviour differed in the two running directions causing differences in the number of traversals reaching behaviour criteria. b, Plot comparing average branch-spike prevalence of two distinct place fields in the same place cells (black) or of in-place field versus out-of-place field somatic firing in the same cells (green). Source data

Extended Data Figure 9 Place field spatial precision is correlated to place field stability.

a, Schematic showing single-plane imaging of the same population of cell somata over multiple days (1, 2 and 8). b, Population images with place cells colour coded by their place field location. Top and bottom rows show place cells in the negative and positive track running directions, respectively. Examples of place cell field fate shown at right: transitory fields occurring on day 1 only (indicated with a minus symbol on the right; black arrows on the left), fields persisting for at least one day (indicated by asterisks on right, white open arrowheads on left) or seven days (indicated by double asterisks on right; white arrows on left); no symbol indicates that the field did not meet the criteria for inclusion (Methods). c, Mean fields of the same cell measured over different days with COM locations from day 1 (bottom; black circles) indicating a precise place field. d, Spatial precision is significantly higher in stable versus transitory place fields (0.127 ± 0.016 cm−1 versus 0.065 ± 0.007 cm−1, respectively; t-test; P = 0.0003). In d, individual data points are depicted by circles to the right of bars and error bars represent s.e.m. Source data

Extended Data Figure 10 Examples of dissociation between somatic firing and branch spiking in a place cell.

a, ΔF/F traces from the (co-acquired) soma and numbered dendritic branches of a place cell during the same imaging session demonstrate that somatic firing and branch spiking are often dissociated. b, Plot of somatic firing intensity versus branch-spike prevalence for all individual place field traversals from all cells (open circles) and binned (solid circles; error bars represent s.e.m.). Branch spiking did not strongly correlate with mean (binned) somatic firing intensity (Spearman’s rank correlation coefficient: P = 0.04; ρ = 0.57). Source data

Supplementary information

Supplementary Information

This file contains Supplementary Notes and additional references. (PDF 215 kb)

Somatic, axonal and dendritic place field transients

Time-series video from two different place cells in different mice (see Figures for scale; Figs 2c and 1b for first and second place cell, respectively). In each cell, time-series videos from somatic and dendritic imaging planes were co-acquired (at 10.4 frames/sec in each plane; planes separated by 70 and 85 μm for first and second place cell, respectively). The time series from each of the imaging planes are aligned in time and vertically concatenated for presentation (displayed at 20 frames/sec). Each somatic (and axonal/dendritic) transient occurs during a separate place field traversal. Note the variability in branch spiking across the visible dendritic branches and the similarity in somatic and axonal (second place cell) transients between the different place field traversals. (MP4 11152 kb)

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Sheffield, M., Dombeck, D. Calcium transient prevalence across the dendritic arbour predicts place field properties. Nature 517, 200–204 (2015). https://doi.org/10.1038/nature13871

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