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A hippocampal network for spatial coding during immobility and sleep

View Article: PubMed Central - PubMed

ABSTRACT

How does an animal know where it is when it stops moving? Hippocampal place cells fire at discrete locations as subjects traverse space, thereby providing an explicit neural code for current location during locomotion. In contrast, during awake immobility, the hippocampus is thought to be dominated by neural firing representing past and possible future experience. The question of whether and how the hippocampus constructs a representation of current location in the absence of locomotion has stood unresolved. Here we report that a distinct population of hippocampal neurons, located in the CA2 subregion, signals current location during immobility, and furthermore does so in association with a previously unidentified hippocampus-wide network pattern. In addition, signaling of location persists into brief periods of desynchronization prevalent in slow-wave sleep. The hippocampus thus generates a distinct representation of current location during immobility, pointing to mnemonic processing specific to experience occurring in the absence of locomotion.

No MeSH data available.


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Spatial firing of CA1, CA2, and CA3 unitsFor the analyses in a and b, unit sample sizes are the same as in Fig. 3b. a, Spatial coverage at different speed cutoffs (mean ± s.e.m.), in which only data from periods satisfying the speed condition were analyzed. For each speed cutoff, a firing rate threshold of 2 Hz was used. The all speeds condition is the same as in Fig. 3b. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p = 0.0015 for all speeds, p = 0.0021 for >4 cm/s, and p < 10-5 for >20 cm/s. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-6 for all speeds, p < 10-7 for >4 cm/s, and p < 10-8 for >20 cm/s. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001. b, Spatial coverage at different firing rate thresholds (mean ± s.e.m.). For each threshold level, spikes at all speeds were analyzed. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-5 for >0.5 Hz, p = 0.0015 for >2 Hz, and p = 0.11 for >5 Hz. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-4 for >0.5 Hz, p < 10-6 for >2 Hz, and p < 10-7 for >5 Hz. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001, n.s., not significant at p < 0.05. c, Example spatial firing maps for CA1, CA3, CA2 P, and CA2 N units. Each column corresponds to data from an individual unit from a single 15-minute task epoch. Upper row: raw maps showing positions visited by the subject (grey) and positions where the unit fired (colored opaque points, plotted chronologically and with darker color values at lower speeds). The total number of spikes (outside of SWRs) in the epoch is reported at upper right. Lower two rows: occupancy-normalized firing maps, with the first row showing maps generated from data from outbound trajectories (center to left or right arms) and the second row inbound trajectories (left or right to center arm; Extended Data Fig. 1a). The spatial peak firing rate (highest rate for a occupancy-normalized bin) is shown at upper right. Shown are data from each unit's highest mean firing rate task epoch. Data from SWR periods were excluded from all plots. Notably, N units could show substantial firing at locations distinct from the reward wells (N unit examples with spike counts of 534, 497, 957, 1819, 668, 1016, 372).
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Figure 4: Spatial firing of CA1, CA2, and CA3 unitsFor the analyses in a and b, unit sample sizes are the same as in Fig. 3b. a, Spatial coverage at different speed cutoffs (mean ± s.e.m.), in which only data from periods satisfying the speed condition were analyzed. For each speed cutoff, a firing rate threshold of 2 Hz was used. The all speeds condition is the same as in Fig. 3b. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p = 0.0015 for all speeds, p = 0.0021 for >4 cm/s, and p < 10-5 for >20 cm/s. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-6 for all speeds, p < 10-7 for >4 cm/s, and p < 10-8 for >20 cm/s. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001. b, Spatial coverage at different firing rate thresholds (mean ± s.e.m.). For each threshold level, spikes at all speeds were analyzed. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-5 for >0.5 Hz, p = 0.0015 for >2 Hz, and p = 0.11 for >5 Hz. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-4 for >0.5 Hz, p < 10-6 for >2 Hz, and p < 10-7 for >5 Hz. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001, n.s., not significant at p < 0.05. c, Example spatial firing maps for CA1, CA3, CA2 P, and CA2 N units. Each column corresponds to data from an individual unit from a single 15-minute task epoch. Upper row: raw maps showing positions visited by the subject (grey) and positions where the unit fired (colored opaque points, plotted chronologically and with darker color values at lower speeds). The total number of spikes (outside of SWRs) in the epoch is reported at upper right. Lower two rows: occupancy-normalized firing maps, with the first row showing maps generated from data from outbound trajectories (center to left or right arms) and the second row inbound trajectories (left or right to center arm; Extended Data Fig. 1a). The spatial peak firing rate (highest rate for a occupancy-normalized bin) is shown at upper right. Shown are data from each unit's highest mean firing rate task epoch. Data from SWR periods were excluded from all plots. Notably, N units could show substantial firing at locations distinct from the reward wells (N unit examples with spike counts of 534, 497, 957, 1819, 668, 1016, 372).

Mentions: We next assessed whether N units showed spatial firing. We found that N units showed less spatial coverage than the other unit populations (Fig. 3a, b, Extended Data Fig. 4). In contrast, CA2 P units typically showed large spatial fields, consistent with recent reports29-31.


A hippocampal network for spatial coding during immobility and sleep
Spatial firing of CA1, CA2, and CA3 unitsFor the analyses in a and b, unit sample sizes are the same as in Fig. 3b. a, Spatial coverage at different speed cutoffs (mean ± s.e.m.), in which only data from periods satisfying the speed condition were analyzed. For each speed cutoff, a firing rate threshold of 2 Hz was used. The all speeds condition is the same as in Fig. 3b. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p = 0.0015 for all speeds, p = 0.0021 for >4 cm/s, and p < 10-5 for >20 cm/s. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-6 for all speeds, p < 10-7 for >4 cm/s, and p < 10-8 for >20 cm/s. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001. b, Spatial coverage at different firing rate thresholds (mean ± s.e.m.). For each threshold level, spikes at all speeds were analyzed. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-5 for >0.5 Hz, p = 0.0015 for >2 Hz, and p = 0.11 for >5 Hz. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-4 for >0.5 Hz, p < 10-6 for >2 Hz, and p < 10-7 for >5 Hz. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001, n.s., not significant at p < 0.05. c, Example spatial firing maps for CA1, CA3, CA2 P, and CA2 N units. Each column corresponds to data from an individual unit from a single 15-minute task epoch. Upper row: raw maps showing positions visited by the subject (grey) and positions where the unit fired (colored opaque points, plotted chronologically and with darker color values at lower speeds). The total number of spikes (outside of SWRs) in the epoch is reported at upper right. Lower two rows: occupancy-normalized firing maps, with the first row showing maps generated from data from outbound trajectories (center to left or right arms) and the second row inbound trajectories (left or right to center arm; Extended Data Fig. 1a). The spatial peak firing rate (highest rate for a occupancy-normalized bin) is shown at upper right. Shown are data from each unit's highest mean firing rate task epoch. Data from SWR periods were excluded from all plots. Notably, N units could show substantial firing at locations distinct from the reward wells (N unit examples with spike counts of 534, 497, 957, 1819, 668, 1016, 372).
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Figure 4: Spatial firing of CA1, CA2, and CA3 unitsFor the analyses in a and b, unit sample sizes are the same as in Fig. 3b. a, Spatial coverage at different speed cutoffs (mean ± s.e.m.), in which only data from periods satisfying the speed condition were analyzed. For each speed cutoff, a firing rate threshold of 2 Hz was used. The all speeds condition is the same as in Fig. 3b. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p = 0.0015 for all speeds, p = 0.0021 for >4 cm/s, and p < 10-5 for >20 cm/s. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-6 for all speeds, p < 10-7 for >4 cm/s, and p < 10-8 for >20 cm/s. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001. b, Spatial coverage at different firing rate thresholds (mean ± s.e.m.). For each threshold level, spikes at all speeds were analyzed. CA2 P > each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-5 for >0.5 Hz, p = 0.0015 for >2 Hz, and p = 0.11 for >5 Hz. CA2 N < each other unit population, Kruskal-Wallis ANOVA, Tukey's post hoc tests, p < 10-4 for >0.5 Hz, p < 10-6 for >2 Hz, and p < 10-7 for >5 Hz. Asterisks: **, p < 0.01; ***, p < 0.001 or p ≪ 0.001, n.s., not significant at p < 0.05. c, Example spatial firing maps for CA1, CA3, CA2 P, and CA2 N units. Each column corresponds to data from an individual unit from a single 15-minute task epoch. Upper row: raw maps showing positions visited by the subject (grey) and positions where the unit fired (colored opaque points, plotted chronologically and with darker color values at lower speeds). The total number of spikes (outside of SWRs) in the epoch is reported at upper right. Lower two rows: occupancy-normalized firing maps, with the first row showing maps generated from data from outbound trajectories (center to left or right arms) and the second row inbound trajectories (left or right to center arm; Extended Data Fig. 1a). The spatial peak firing rate (highest rate for a occupancy-normalized bin) is shown at upper right. Shown are data from each unit's highest mean firing rate task epoch. Data from SWR periods were excluded from all plots. Notably, N units could show substantial firing at locations distinct from the reward wells (N unit examples with spike counts of 534, 497, 957, 1819, 668, 1016, 372).
Mentions: We next assessed whether N units showed spatial firing. We found that N units showed less spatial coverage than the other unit populations (Fig. 3a, b, Extended Data Fig. 4). In contrast, CA2 P units typically showed large spatial fields, consistent with recent reports29-31.

View Article: PubMed Central - PubMed

ABSTRACT

How does an animal know where it is when it stops moving? Hippocampal place cells fire at discrete locations as subjects traverse space, thereby providing an explicit neural code for current location during locomotion. In contrast, during awake immobility, the hippocampus is thought to be dominated by neural firing representing past and possible future experience. The question of whether and how the hippocampus constructs a representation of current location in the absence of locomotion has stood unresolved. Here we report that a distinct population of hippocampal neurons, located in the CA2 subregion, signals current location during immobility, and furthermore does so in association with a previously unidentified hippocampus-wide network pattern. In addition, signaling of location persists into brief periods of desynchronization prevalent in slow-wave sleep. The hippocampus thus generates a distinct representation of current location during immobility, pointing to mnemonic processing specific to experience occurring in the absence of locomotion.

No MeSH data available.


Related in: MedlinePlus