Volume 27, Issue 23, Pages e4 (December 2017)

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Volume 27, Issue 23, Pages 3658-3665.e4 (December 2017) Consistency of Spatial Representations in Rat Entorhinal Cortex Predicts Performance in a Reorientation Task  Shahaf Weiss, Ghadeer Talhami, Xenia Gofman-Regev, Sophia Rapoport, David Eilam, Dori Derdikman  Current Biology  Volume 27, Issue 23, Pages 3658-3665.e4 (December 2017) DOI: 10.1016/j.cub.2017.10.015 Copyright © 2017 Elsevier Ltd Terms and Conditions

Figure 1 Experimental Design and Behavioral Results (A) Histological preparation. Tetrode trace in MEC is shown (red circle). (B) Layout of apparatus. Example of corner choices for a single recording day is shown (the correct corner location was changed between recording days), color-coded for illustration purposes—blue for correct choice, light blue for near error, light red for far error, and red for rotational error. (C) A typical example of a trajectory in A, first open-field recording; B, task session; and A’, second open-field recording. (D) Schematic representation of a reorientation task session. (E) Ratios of task performance scores for different corner choices. The chance level for choice among four corners is 25%. C, correct; F, far error; N, near error; R, rotational error. Before disorientation, there was a clear difference between correct and rotational choice ratios as noted above; following disorientation, there was no significant difference between both corner choices (H0: equal ratios between correct and rotational corner choices; χ2 = 0.4763; df = 1; p = 0.49). The ratio of geometrically identical corner choices (correct and rotational) versus non-geometrically identical corner choices (near and far) did not differ significantly before and after disorientation (χ2 = 3.208; df = 1; p = 0.073). However, this ratio was significantly different from a null hypothesis stating that corner choice was not affected by geometry (H0: equal ratios between geometrically identical versus non-identical corners; χ2 = 31.827; df = 1; p < 0.0001). Similar findings were obtained for task engagement parameters (Figure S1B). (F) The stability of behavioral outcomes within trial blocks. Blue bars, population of 1,000 permutated trials; red line, the observed proportion of same sign trials (positive or negative performance scores). (G) The position-triggered mean task performance scores for all trial blocks (mean ± SEM) considering only correct and rotational choices. ∗p < 0.05. Within blocks, the mean task performance improved from 0.23 ± 0.06 in the second trial to 0.41 ± 0.08 in the third trial (Wilcoxon signed-rank test; z = −2.08; p < 0.05). See also Figures S1 and S2. Current Biology 2017 27, 3658-3665.e4DOI: (10.1016/j.cub.2017.10.015) Copyright © 2017 Elsevier Ltd Terms and Conditions

Figure 2 Response of HD Cells and Grid Cells to Disorientation (A and B) Examples of head-direction (HD) cell and grid cell activity during open-field versus task sessions. (A) Responses of two HD cells are shown. Each panel depicts HD (black) over time and HD during spike times (red) in a random foraging session versus a task session. The bottom part of each panel depicts the HD and spike times during the reorientation task. Black horizontal bars indicate periods of disorientation epochs. Yellow bars indicate periods between disorientation episodes. Blue bars indicate correct trials, light-blue bars indicate near error trials, red bars indicate rotational error trials, and light-red bars indicate far error trials. (B) Rate maps of two grid cells are shown. Top and third rows, rate map of open-field, random foraging session, and a 180° rotated version of the same rate map; second and fourth rows, rate maps of four trial blocks, showing rotation of the grid between blocks while maintaining the overall grid structure. (C and D) Visualization of orientation scores in the task for simultaneously recorded HD cells (C) and grid cells (D). Each square represents a single trial, color coded according to the HD orientation score observed during that trial. Scores are scaled from +1 (blue) to −1 (red); trials in which the firing rate was under 0.05 Hz are marked in black. Yellow lines represent disorientation events between trials. Population vector and task scores for corresponding trials are displayed below each panel. (E and F) The stability of orientation scores for HD (E) and grid cells (F) within blocks. The observed proportion of same sign trials (red line) versus 1,000 permutations of trials from different blocks (blue bars) is shown. See also Figures S1, S2, and S4. Current Biology 2017 27, 3658-3665.e4DOI: (10.1016/j.cub.2017.10.015) Copyright © 2017 Elsevier Ltd Terms and Conditions

Figure 3 Simultaneously Recorded HD Cells and Grid Cells Share Orientation of Alignment (A) HD scores and grid orientation population vector scores for all trials with simultaneously recorded cells of both types. (B) Same as (A) but only for trials immediately following disorientation events. (C) Trial-by-trial visualization of HD and grid orientation scores during three recording sessions (asterisks mark conjunctive HD × grid cells) for simultaneously recorded cells. Scores are scaled from +1 (blue) to −1 (red). Trials in which the firing rate was under 0.05 Hz are marked in black. Yellow vertical lines represent disorientation events between trials. See also Figures S1, S2, and S4. Current Biology 2017 27, 3658-3665.e4DOI: (10.1016/j.cub.2017.10.015) Copyright © 2017 Elsevier Ltd Terms and Conditions

Figure 4 The Probability of a Behavioral Outcome Depends on Current and Past Trial Population Vectors of HD or Grid Orientation Scores An increase in probability for correct corner choice was found in cases of properly aligned HD or grid representations over multiple trials. For each data point, the probability of choice was compared to the probability observed without considering population vectors from previous trials. See also Figures S1–S3. (A) The probability of a correct corner choice, given a positive HD population vector in the current trial, and a positive (blue) or negative (cyan) population vector in the previous n trials (“instances of past state”). ∗p < 0.05; ∗∗p < 0.01. (B) The probability of a correct corner choice, given a negative HD population vector in the current trial, and a negative (red) or positive (pink) population vector in the previous n trials. (C) The probability of a correct corner choice, given a positive grid population vector in the current trial. Color code is similar to (A). (D) The probability of a correct corner choice, given a negative grid population vector in the current trial. Color code is similar to (B). Current Biology 2017 27, 3658-3665.e4DOI: (10.1016/j.cub.2017.10.015) Copyright © 2017 Elsevier Ltd Terms and Conditions