Hippocampal place cells construct reward related sequences through unexplored space
- University College London, United Kingdom
Figures
Figure 1 with 4 supplements
Preferential preplay of a behaviourally relevant, unvisited environment.
(A) Experimental protocol. (i) Prior to running on the track, the animals rested for at least an hour (REST1). (ii) Following REST1, animals ran 20 laps on the stem (RUN1). Access to the arms was …
Figure 1—figure supplement 1
Schematic of experimental apparatus black rectangles on track represent texture cues, dotted line transparent barrier, circle rest enclosure (18 cm wide), wiggly border demarcates the white curtains surrounding the environment, with distal landmarks fixed to the curtain (‘X’ and ‘0’).
Note, the rest enclosure was only present during rest periods.
Figure 1—figure supplement 2
Ripple power is elevated during preplay events power in the ripple spectrum (80–250 Hz) is higher during preplay events (red) than during both non-significant spiking events (black, p < 0.001) and non-event periods (dashed line, p < 0.001).
Vertical lines represent start and end of spiking events.
Figure 1—figure supplement 3
Place cell templates place cell sequences for each template.
Cells are ordered according to the location of their place field. x-axis shows location on arm (cm)—left side closer to the stem, and y-axis cell IDs. UCA = Up Cued Arm, DCA = Down Cued Arm, UUA = …
Figure 1—figure supplement 4
Spiking events for cued arm in REST2 centre: bootstrapped cumulative distribution of (absolute) correlations between spiking events and the cued template in REST2 (red = data, black = shuffle).
Lighter areas of the curve show 1 standard deviation of the mean. Raster plots: spiking events of varying correlations with the future cued arm template. The title of each quadrant shows the …
Figure 2 with 2 supplements
Preplay is a function of goal-cueing.
(A) Bootstrapped cumulative distribution of (absolute) correlations between spiking events and the cued template in REST2 (red = data, black = shuffle). Lighter areas of the curve show 1 standard …
Figure 2—figure supplement 1
Preplay of cued arm in REST2—distribution-based analysis A mean difference between the bootstrapped cumulative distributions of absolute correlations for the data and the bootstrapped shuffle for the cued and uncued arms in REST2 and the cued arm in REST1.
If a place cell template is preplayed then the AUC of the data distribution should be smaller than that of the shuffled distribution (i.e., negative difference score). To assess significance we …
Figure 2—figure supplement 2
Preplay of stem during REST1 bootstrapped cumulative distribution of absolute correlations for spiking events of the stem, recorded during REST1.
Green line shows the data and the black line the bootstrapped distribution obtained after shuffling events 100 times. Light green regions show 1 standard deviation of the distribution. Inset: …
Figure 3 with 4 supplements
Spatial and temporal dynamics of preplay.
(A) The proportion of preplay events when negative (‘reverse’) and positive (‘forward’) spiking event correlations are analysed separately. Bars show means for all data and black lines the results …
Figure 3—figure supplement 1
Preplay of cued arm during GOAL-CUE—distribution-based analysis A mean difference between the cumulative distributions of absolute correlations for the bootstrapped data and shuffle for the cued and uncued arms during GOAL-CUE.
If a place cell template is preplayed then AUC of the data distribution should be smaller than that of the shuffled distribution (i.e., negative difference score). To assess significance we computed …
Figure 3—figure supplement 2
Preferential preplay of the cued arm is not confounded by the number and activity of cells on the cued arm.
(A) Proportion of preplay events for the cued and uncued arm in REST2 following down-sampling to equate the number of cells on the two arms. Bars show means, black lines the results for individual …
Figure 3—figure supplement 3
Animals' interest in cued arm during GOAL-CUE is associated with subsequent preplay for each animal.
The proportion of preplay events for the cued arm recorded during REST2 is shown plotted against that animal's interest in the cued arm assessed by body position during GOAL-CUE. −0 indicates animal …
Figure 3—figure supplement 4
Tetrode tracts example histology showing the location of tetrode recording from area CA1 in rat R504.
Staining: cresyl violet.
Figure 4
Bayesian reconstruction confirms preferential cued arm preplay.
(A–B) Confusion matrices based on RUN2 data showing decoding accuracy for the cued (A) and uncued arms (B). Columns show the mean posterior probability distribution across the arm ordered by the …
Tables
Table 1
Experimental parameters
| R1838 | R505 | R584 | R504 | All rats (mean) | |
|---|---|---|---|---|---|
| Cue bias (dwell time) | |||||
| RUN1 | 0.33 | 0.32 | −0.05 | −0.20 | 0.10 |
| GOAL-CUE | 0.46 | 0.20 | 0.31 | 0.32 | 0.33 |
| Cue bias (looking time) | |||||
| RUN1 | −0.09 | −0.02 | 0.01 | −0.36 | −0.11 |
| GOAL-CUE | 0.06 | 0.31 | 0.09 | 0.05 | 0.13 |
| RUN2 arm bias | |||||
| RUN2 | 1.0 | 0.84 | 1.0 | 1.0 | 0.96 |
| Session duration (min) | |||||
| SLEEP1 | 60 | 88 | 75 | 74 | 74 |
| RUN1 | 13 | 10 | 13 | 9 | 11 |
| GOAL-CUE | 10 | 17 | 12 | 11 | 13 |
| SLEEP2 | 60 | 67 | 71 | 60 | 65 |
| RUN2 | 34 | 19 | 35 | 31 | 30 |
| Template length (number of cells) | |||||
| Up cued arm | 20 | 36 | 53 | 43 | 38 |
| Down cued arm | 15 | 35 | 45 | 33 | 32 |
| Up uncued arm | 19 | 26 | 45 | 40 | 33 |
| Down uncued arm | 15 | 32 | 41 | 43 | 33 |
Table 2
REST period results
| Animal | Arm | # spiking events | # preplay events | % preplay | % chance | p-value |
|---|---|---|---|---|---|---|
| REST2 | ||||||
| R1838 | Cued | 44 | 9 | 20.45 | 6.86 | 6.56 × 10−4 |
| Uncued | 26 | 3 | 11.54 | 6.77 | 0.10 | |
| R505 | Cued | 631 | 38 | 6.02 | 4.57 | 0.037 |
| Uncued | 860 | 29 | 3.37 | 3.82 | 0.72 | |
| R584 | Cued | 437 | 32 | 7.32 | 4.73 | 6.20 × 10−3 |
| Uncued | 398 | 22 | 5.53 | 4.74 | 0.19 | |
| R504 | Cued | 516 | 41 | 7.95 | 5.15 | 0.0027 |
| Uncued | 373 | 19 | 5.09 | 4.40 | 0.21 | |
| All rats | Cued | 1628 | 120 | 7.37 | 4.86 | 4.12 × 10−6 |
| Uncued | 1657 | 73 | 4.41 | 4.22 | 0.33 | |
| REST1 | ||||||
| R1838 | Cued | 63 | 3 | 4.76 | 7.05 | 0.66 |
| Uncued | 35 | 2 | 5.71 | 7.37 | 0.48 | |
| R505 | Cued | 664 | 39 | 5.87 | 4.34 | 0.025 |
| Uncued | 1215 | 38 | 3.13 | 3.45 | 0.70 | |
| R584 | Cued | 269 | 14 | 5.20 | 4.67 | 0.28 |
| Uncued | 247 | 21 | 8.50 | 4.72 | 0.0035 | |
| R504 | Cued | 311 | 6 | 1.93 | 4.44 | 0.99 |
| Uncued | 173 | 11 | 6.36 | 4.21 | 0.063 | |
| All rats | Cued | 1307 | 62 | 4.74 | 4.56 | 0.34 |
| Uncued | 1670 | 72 | 4.31 | 3.80 | 0.12 | |
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Summary results from REST1 and REST2 for the cued and uncued arms for individual animals. # Spiking events = total number of spiking events recorded. # preplay events = number of significant spiking events. % preplay = Proportion of the spiking events that qualified as preplay events (i.e., that were significant), expressed as a percentage. % chance = proportion of spiking events from the shuffled data that qualified as preplay events, expressed as a percentage. p-value = probability, derived from a binomial test, of obtaining the observed number of preplay events for each template given the chance level calculated from the shuffled data.
Table 3
REST1 stem results
| Animal | # spiking events | # preplay events | % preplay | % chance | p-value |
|---|---|---|---|---|---|
| R1838 | 68 | 3 | 4.41 | 6.01 | 0.59 |
| R505 | 980 | 35 | 3.57 | 4.03 | 0.74 |
| R584 | 329 | 17 | 5.17 | 4.53 | 0.24 |
| R504 | 396 | 18 | 4.55 | 3.50 | 0.11 |
| All rats | 1773 | 73 | 4.12 | 4.08 | 0.44 |
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Summary results from REST1 analysing preplay of the stem. # Spiking events = total number of spiking events recorded. # Preplay events = number of significant spiking events. % preplay = Proportion of the spiking events that qualified as preplay events (i.e., that were significant), expressed as a percentage. % chance = proportion of spiking events from the shuffled data that qualified as preplay events, expressed as a percentage. p-value = probability, derived from a binomial test, of obtaining the observed number of preplay events for each template given the chance level calculated from the shuffled data.
Table 4
GOAL-CUE results
| Animal | Arm | # spiking events | # preplay events | % preplay | % chance | p-value |
|---|---|---|---|---|---|---|
| R1838 | Cued | 5 | 0 | 0 | 7 | 0.30 |
| Uncued | 5 | 0 | 0 | 7 | 0.30 | |
| R505 | Cued | 45 | 3 | 6.67 | 4.02 | 0.11 |
| Uncued | 48 | 1 | 2.08 | 3.57 | 0.52 | |
| R584 | Cued | 111 | 8 | 7.21 | 4.81 | 0.087 |
| Uncued | 112 | 5 | 4.46 | 4.82 | 0.46 | |
| R504 | Cued | 11 | 0 | 0 | 4.36 | 0.39 |
| Uncued | 7 | 1 | 14.29 | 5.00 | 0.044 | |
| All rats | Cued | 172 | 11 | 6.40 | 4.64 | 0.11 |
| Uncued | 170 | 7 | 4.12 | 4.49 | 0.50 |
-
Summary results from GOAL-CUE analysis # Spiking events = total number of spiking events recorded. # Preplay events = number of significant spiking events. % preplay = Proportion of the spiking events that qualified as preplay events (i.e., that were significant), expressed as a percentage. % chance = proportion of spiking events from the shuffled data that qualified as preplay events, expressed as a percentage. p-value = probability, derived from a binomial test, of obtaining the observed number of preplay events for each template given the chance level calculated from the shuffled data.
