New Experiences Enhance Coordinated Neural Activity in the Hippocampus

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New Experiences Enhance Coordinated Neural Activity in the Hippocampus Sen Cheng, Loren M. Frank  Neuron  Volume 57, Issue 2, Pages 303-313 (January 2008) DOI: 10.1016/j.neuron.2007.11.035 Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 1 Background and Experimental Setup The schematic of the experimental setup shows a sample sequence of different T maze configurations that were used in the experiment. In any given session, only three out of the eight arms were accessible; closed arms are shown in gray outline. Only data that were obtained when animals were located on the outer arms indicated by filled bars were analyzed. The color scheme is maintained throughout the paper, with the exception of Figure 8: pretraining maze configuration (gray), familiar arm in session 2 (black), and novel arm in session 2 on days 1, 2, and 3 of novel exposure (red, green, and blue, respectively). Each novel configuration was used for 2 or 3 days. Scale: the length of one arm is 75 cm. Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 2 Increased Correlations between Novel Arm Cell Pairs Due to Spiking within HFEs (A) CCG using all spikes for cell pairs recorded on different tetrodes on novel day 1 with place fields in familiar (top) and novel (bottom) arm. Shown are the raw CCG (gray line), a smoothed CCG using a Gaussian kernel (SD 5 ms, solid red and black lines), and the envelope of the CCG (smoothed with a Gaussian kernel with SD 250 ms, dashed red and black lines). The difference, measured at the points indicated by the arrows, is the excess correlation (see Experimental Procedures). (B) Cumulative distribution of excess correlation values in the population using all spikes. Novel arm cell pairs had higher excess correlation on day 1 (rank-sum test, n = 78, p = 1.8 × 10−4) and day 2 (n = 22, p = 0.035), but not on day 3 (n = 37, p = 0.74), than did the familiar arm cell pairs (all days pooled, n = 86). (C) Differences in excess correlation between novel and familiar arm cell pairs disappeared when only spikes fired within place fields were included (p's > 0.38). (D) Sample of ripple with high peak amplitude of mean + 28.2 SD (top) and HFEs with low amplitude of mean + 3.9 SD (bottom). Ripple or HFE events are indicated by red lines above LFP traces (gray, raw signal; black,band-filtered [150–250 Hz] signal). Scale: LFP traces are 500 ms long, top red bar is ∼80 ms. (E) Excluding spikes fired during HFEs abolished the difference in excess correlation (p's > 0.30). Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 3 Increased Number of HFEs and Increased Spiking during HFEs (A) Average numbers of HFEs per second that the animal spent in the novel arm (red, green, and blue bars) and in the familiar arm (black bars) across 3 days of novel exposure. (B) Mean duration of HFEs. (C and D) Number of spikes during HFEs divided by the number of HFEs, averaged across cells. “Place field arm” (C) is the novel arm for novel arm cells and familiar arm for familiar arm cells; “non-place-field arm” (D) is the other arm. Error bars represent standard errors. Symbols indicate results of rank-sum test (∗p < 0.05, ∗∗p < 0.01, ∗∗∗p < 0.001). Only within-day planned comparisons were performed. Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 4 Novel Arm Cells Were Initially More Likely to Be Active and More Coordinated during HFEs Activity of cell assemblies representing the novel (red, green, and blue bars) and familiar arm (black bars) when animal was located on the place field and non-place-field arm. (A and B) The probability of cells being active during a given HFE; (C and D) average number of spikes fired per activation; (E and F) the probability of cell pairs being coactive; (G and H) the strength of the coordination of the coactivity measured as a z score (see Experimental Procedures). Error bars represent standard errors. Symbols indicate results of rank-sum test (∗p < 0.05, ∗∗p < 0.01, ∗∗∗p < 0.001). Only within-day planned comparisons were performed. Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 5 Spiking of Novel Arm Cells during HFEs Was More Precisely Timed (A) Smoothed CCG using only spikes that occurred during HFEs for two cell pairs with place fields on familiar (top) and novel (bottom) arm (see Experimental Procedures). The rms time lag was computed from the CCG between time lags of ±100 ms (gray-shaded areas). In these examples, the rms time lags of the familiar and novel arm cell pairs are 41 ms and 27 ms, respectively. (B) Cumulative distribution of rms time lags across the population. Temporal coordination of novel arm cell pairs during HFEs was more precise on day 1 (rank-sum test, n = 77, p = 4.2 × 10−5) and day 2 (n = 18, p = 6.3 × 10−4) than that of familiar arm cell pairs (n = 27), but not on day 3 (n = 27, p = 0.17). Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 6 Phase Precession in the Novel Arm Was Not More Coordinated (A) Phase precession snapshot for one place field in the novel arm on day 1. Shown is the position-phase response after the animal spent 20 s in the novel arm. The colorbar (arbitrary units) represents the likelihood of spiking. The full evolution of this neuron's firing across day 1 is shown in Movie S1. (B) Mean phase precession strength across all identified place fields within the first three minutes that the animal spend in the novel arm on day 1 (red), day 2 (green), and day 3 (blue), and in the familiar arm (black). The error bars indicate standard errors. Only within-day planned comparisons were performed (rank-sum test, day 1: p = 0.014, days 2 and 3: p > 0.72). Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 7 Sequence Compression in Novel Arm Cell Pairs Was Not More Reliable (A) Schematic firing rate maps of three cells with overlapping place fields. Colored areas indicated elevated firing rate. Each cell shows phase precession that facilitates compression of behavioral sequences to spike sequences within one theta cycle. (B) The theta time scale separation between a pairs' spiking is determined from the location of the highest peak in the crosscorrelogram within ±100 ms (CCG peak indicated by arrow). (C) Sequence compression for familiar arm cell pairs (all days combined, n = 64). (D–F) Sequence compression for novel arm cell pairs on (D) day 1 (n = 78), (E) day 2 (n = 18), and (F) day 3 (n = 40). The SCI was significantly lower in the novel arm than in the familiar arm on day 1 (z test, p = 0.003) and day 2 (p = 0.001), but not on day 3 (p = 0.70). Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions

Figure 8 Neural Representation of the Familiar Arm Remained Stable Unlike elsewhere in this paper, red, green, and blue represent familiar arm cells on days 1, 2, and 3, respectively. (A) Mean phase precession strength across all identified place fields within the first 3 min that the animal spend in the outer arms of the pretraining configuration (gray) and in the familiar arm of session 2 on days 1–3. The error bars indicated standard errors. No pairwise comparison shows a significant difference (rank-sum test, p > 0.65). (B) The SCI in familiar arm cell pairs (Figure 7C) was not significantly different from SCI in the pretraining maze configuration shown here (n = 179, z test, p = 0.48). (C) Excess correlation in familiar arm cell pairs was not significantly different from excess correlation in the pretraining maze configuration (gray, n = 232) on day 1 (rank-sum, n = 26, p = 0.17) and day 2 (n = 18; p = 0.78). On day 3 the difference is significant (n = 42, p = 0.041) at the 0.05-level; however, the difference in excess correlation is very small. There were no significant differences between any two individual days (rank-sum, pairwise comparisons, p > 0.22). Neuron 2008 57, 303-313DOI: (10.1016/j.neuron.2007.11.035) Copyright © 2008 Elsevier Inc. Terms and Conditions