Social place-cells in the bat hippocampus

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Science  12 Jan 2018:
Vol. 359, Issue 6372, pp. 218-224
DOI: 10.1126/science.aao3474
  • Fig. 1 Neurons in bat hippocampal area CA1 represent the position of conspecifics.

    (A) Behavioral setup inside a flight room (2.30 by 2.69 by 2.56 m). The demonstrator bat (blue) was trained to fly from the start ball, roughly randomly to either ball A or ball B, and back, and the observer bat had to imitate this flight. Two different trials are shown, one to ball A (trial i) and one to ball B (trial j). (B) Coronal section through dorsal hippocampus of one observer bat. Arrowhead, electrolytic lesion at end of tetrode track. (C) Five example cells (top view). For each cell, the left column shows the place-cell representation, based on spikes from the observer’s neuron and the self-flight-trajectories of the observer (Self), and the right column shows the social place-cell representation, based on spikes from the same observer’s neuron, plotted together with the demonstrator’s trajectories (Demo.). (Top) Flight trajectories (gray) with spikes overlaid (red). A, B, and S are landing balls A, B, and start ball; arrows denote flight-direction (↑, flying away from start-ball; ↓, flying toward the start ball). (Bottom) Firing-rate maps. Color scale ranges from zero (blue) to maximal firing rate (red; value indicated). The four leftmost cells are social place-cells; some of these neurons are also place-cells (cells 358, 254, and 52), and some are not (cell 266). Cell 313 is a “pure” place cell. Correlations between the firing-rate maps for self and other are indicated for each cell (correlations are undefined for cells 266 and 313 because one of the maps is flat). Scale bar, 50 cm. (D) Total number of significant social place-cells versus significant classical place cells that we recorded. (E) Number of place cells and social place-cells that were significantly tuned to one flight-direction (↑), the other flight-direction (↓), or both directions (↑↓). Classical place cells are in red (n = 261), and social place-cells are in blue (n = 68). (F) Locations of peak firing for all the significant maps for place cells (red dots, n = 371 cells × directions), and social place-cells (blue dots, n = 76 cells × directions); cells that had significant tuning in both directions were depicted twice; hence, the counts here are larger than in (D). Dots were randomly jittered by up to ±5 cm (half bin) for display purposes. (G) Average peak firing rate for all the classical place cells (red, n = 371 cells × directions) and all the social place-cells (blue, n = 76 cells × directions). **P < 0.01. (H) (Top) Distributions of correlation coefficients between classical place cell maps and social place-cell maps for all the neurons that encoded significantly either self-position or conspecific position and had >20 spikes per map (left histogram) or >300 spikes per map (right histogram). Gray, the data; black lines, cell-shuffling distributions (14). (Bottom) Map correlations increased with firing rate. Error bars, mean ± SEM; gray bars, the data; open bars, cell-shuffling; number of cells × directions included in the four bars: n = 334, 218, 137, and 91; *P < 0.05; **P < 0.01; n.s., nonsignificant.

  • Fig. 2 Coding of conspecific position cannot be explained by self-head-movements of the observer bat nor by trajectory planning.

    (A) Two example traces of flight velocity and acceleration of the observer’s head. (Top) Flight velocities of the two bats. (Middle) Acceleration of observer’s head. g, Earth’s gravitational acceleration. (Bottom) Very low acceleration around the demonstrator’s flight (gray rectangle). (B) Change in head azimuth of the observer (ΔAz) as function of time from onset of demonstrator’s flight. Each example shows data from 1 recording day in one flight direction; these examples correspond to the three cells in (E). Black, demonstrator flights in which the observer’s head moved <1 SD (σ = 20.18°, which corresponds to <6 mm movement; right y axis) (14). Gray, demonstrator flights that included deviant head movements of the observer bat that exceeded ±σ. Numbers indicate proportion of deviant flights out of all the flights on this day. (C) Distribution of ΔAz of the observer’s head, pooled over all days with significant social place-cells where motion-sensor data were recorded (n = 18 days, n = 35,284 samples). Gray lines mark 1 SD (σ = 20.18 o), which was the threshold used in (B) to define deviant flights. (D) Mean firing rate of social place-cells outside the task, triggered on the peak velocity of observer’s head movements, for all the 1-s segments with small angular displacement <20° (n = 14,893 segments, pooled over all significant social place-cells with motion-sensor data; shaded area indicates mean ± SEM). (E) Three example cells, showing high correlation between social place field maps before (top) and after (bottom) removal of all the flights that included observer head-movements [At bottom, we removed all gray-colored flights in (B) and the corresponding spikes]. (F) Blue histogram, distribution of correlation coefficients between social place-cell maps with and without removal of flights with observer movements. Black line, cell-shuffling distribution. We included here all the significant social place-cells where motion-sensor data were recorded (n = 29 cells × directions). Shown are high correlations between maps with versus without removal of flights with observer movements (blue histogram); t test with unequal variances, compared with cell-shuffling control (black): P < 10−26. (G) Example of a SWR. (Top) Spectrogram of the SWR. (Middle) Raw LFP trace (1 to 400 Hz bandpass). Scale bars, 30 ms and 200 μV. (Bottom) Spikes from four simultaneously recorded neurons (red ticks). Same time scale in all panels. (H) (Top) Mean SWR waveform, averaged across all recording days with social place-cells (n = 46 days; n = 9,092 SWRs). (Bottom) SWR-triggered firing rate, averaged over all neurons recorded during days with social place-cells (n = 276 neurons; shaded area, mean ± SEM). (I) Two social place-cells (columns), showing high stability with versus without flights that included SWRs (top versus bottom). (J) Distribution of correlation coefficients between social place-cell maps and the same maps after removal of flights with SWRs. Blue histogram, data for all cells with >20 spikes per map that had SWRs during observer flights (n = 20 cells × directions). Black line, cell-shuffling distribution. t test with unequal variances, data compared with cell-shuffling control: P < 10−140. (K) Two social place-cells (columns), showing high stability in correct trials (top) versus incorrect trials (bottom). (L) Distribution of correlation coefficients between social place-cell maps computed by using correct trials versus incorrect trials. Blue histogram, data for all neurons with >20 spikes per map (n = 43 cells × directions). Black line, cell-shuffling distribution. t test with unequal variances, data compared with cell-shuffling control: P < 10−8. We included in this analysis only cells with >15 correct flights and >15 incorrect flights; n = 43 cells × directions. (M) (Left) Simulated spatial distribution of social place fields, assuming that they are generated by place cell sequences with a ratlike sequence-speed of 8 m/s (14). (Right) Same, using a sequence speed of 43 m/s, which is scaled up to the flight speed of the demonstrator bat (corresponding to 20 times the bat’s flight speed in our task). Blue circles and crosses denote cells with preferred direction ↑ and ↓, respectively.

  • Fig. 3 The representation of conspecifics is allocentric, not egocentric.

    (A and B) Dividing the demonstrator’s flight data based on the observer’s head direction during demonstrator’s flights. (A) Schematic drawing of directional notations of the bat’s head relative to the two landing balls. (B) Distribution of the azimuthal head directions of the observer during demonstrator flights; data from 1 recording day. The median head direction (6.8°) is plotted in red. Direction 0° is parallel to the east-west wall of the room. (C) Two cells showing stability of their social place fields between right-pointing head directions (top) and left-pointing head directions (bottom). (D) Blue histogram, distribution of the correlation coefficients between right-looking maps and left-looking maps (blue), plotted for all the social place-cells for which we recorded motion-sensor data and had >20 spikes per map (n = 24 cells × directions); t test with unequal variances, compared with cell-shuffling control (black): P < 10−4. Black line, cell-shuffling distribution, consisting of correlations between left-looking maps from cell i and right-looking maps from cell j across all the cell pairs where ij. (E) Scatter plot of the similarity between right-looking and left-looking maps (y axis), versus the difference between the means of the right-looking and left-looking angles (x axis). No correlation was found (r = –0.12, P = 0.59; shown is a large span of azimuthal head-direction angles).

  • Fig. 4 The conspecific is represented differently from inanimate moving objects.

    (A) Illustration of the behavioral task that we conducted in two of the four recorded bats. (B) Five example cells, showing firing-rate maps for the position of the demonstrator (left column), the position of the informative object (middle), and the position of the noninformative object (right). Cells 184, 169, and 361 encoded both the conspecific bat and the objects; cell 182 encoded only the objects; and cell 221 encoded only the conspecific. (C) Venn diagram summarizing the numbers of cells that represented significantly the conspecific and the two objects in these two bats. (D) Spatial information rate for all the cells representing significantly the position of the demonstrator (blue), the informative object (green), and the noninformative object (gray). Horizontal lines show the median, boxes show the 25th to 75th percentiles, and vertical lines show the 10th to 90th percentiles. (E) A cell exhibiting a difference in its firing-rate maps between different flight directions of the demonstrator bat (left column), but showing no directionality for the two objects (middle and right columns); compare the top and bottom maps for the two objects (direction ↑ vs ↓). (F) Directionality: population summary. Shown are correlations of firing-rate maps between the two flight directions: for the self-representation, the demonstrator bat, and the informative and noninformative objects (data for all cells in which at least one flight direction exhibited a significant map, and both maps contained >50 spikes per map). The maps are much more directional (lower correlations) for the demonstrator than for the two objects; t test for the correlations between the two directions for demonstrator-bat versus the two pooled objects: *P < 0.05. (G) Correlations of firing-rate maps for demonstrator bat versus informative object (left), demonstrator bat versus noninformative object (middle), and informative object versus noninformative object (right). Correlations here were computed for all cells in which at least one of the two maps was significant, and only for maps with >50 spikes; t test of the object-object similarity versus the conspecific-object similarities: **P < 0.01 for both comparisons. To increase the robustness of comparisons between demonstrator and objects, (C), (D), (F), and (G) included only cells that met a strict criterion of >25 flights per map and >50 spikes per map. (H) Functional anatomy along the proximodistal axis of CA1, for one of the two bats tested with three sessions (14). Shown is the percentage of significant tuning, separately for proximal and distal tetrodes. (Left) Place cells (Self). (Middle) Social place-cells (Demonstrator). (Right) Object place cells (pooled over both objects). ***P < 10−3; ****P < 10−5.

Supplementary Materials

  • Social place-cells in the bat hippocampus

    David B. Omer, Shir R. Maimon, Liora Las, Nachum Ulanovsky

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Figs. S1 to S8
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    Images, Video, and Other Media

    Movie S1
    A movie that illustrates schematically the delayed match-to-place task. Blue color, demonstrator bat. Red color, observer bat (this bat was implanted with a microdrive and equipped with a neural-logger for wireless neural recordings). Bats and landing-balls are not drawn to scale, for illustration purposes.
    Movie S2
    A movie showing video-tracking of the two bats as captured through one of the two cameras in the experiment. Light-emitting diodes (LEDs) were placed on the bats' heads, and were used for tracking. Blue LED, demonstrator bat; Red LED, observer bat. Video-tracker image was smoothed for clarity. Note that the observer bat mimicked the flight-targets of the demonstrator-bat (ball A or ball B): In the first trial the demonstrator bat (blue) flew to ball B (right), and after a delay the observer bat (red) mimicked it and also flew to ball B; subsequently, the demonstrator bat flew to ball A (left), and the observer bat (red) mimicked it again and flew to ball A. Movie sped-up 2x.

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