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A hippocampal network for spatial coding during immobility and sleep

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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.

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N units signal current location during immobilitySpatial firing maps of five example CA2 site units. Each column corresponds to a unit. Upper row: positions visited (grey) and positions where the unit fired (colored points: P units in red, N units in blue). Total number of spikes is reported at upper right. Lower row: occupancy-normalized firing maps. Peak spatial firing rate is reported at upper right. Subjects stopped locomoting at the ends of the maze arms to receive reward and also stopped intermittently elsewhere in the maze (Extended Data Fig. 1a). b, Spatial coverage in the hippocampal unit populations (mean ± s.e.m.; # of units: CA1: 476, CA2 P: 142, CA2 N: 79, CA3: 271). The CA2 N and P unit populations showed the lowest and highest spatial coverages, respectively (Kruskal-Wallis ANOVA, Tukey's post hoc tests, CA2 P > each other population, p = 0.0015; CA2 N < each other population, p < 10-6). Asterisks: **, p < 0.01; ***, p ≪ 0.001. c, Reward well firing of four example CA2 N units. Each column corresponds to a unit. For each well, the last ten visits (in a task recording epoch) are shown. Grey line: time of well entry (t = 0); yellow line: time of reward delivery (omitted in error trials). SWR periods are shown as pink zones. The two leftmost units were recorded simultaneously and on the same tetrode. d, Well specificity distribution in the N unit population. Mean ± s.e.m.: 0.78 ± 0.03 (n = 53 units).
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Figure 13: N units signal current location during immobilitySpatial firing maps of five example CA2 site units. Each column corresponds to a unit. Upper row: positions visited (grey) and positions where the unit fired (colored points: P units in red, N units in blue). Total number of spikes is reported at upper right. Lower row: occupancy-normalized firing maps. Peak spatial firing rate is reported at upper right. Subjects stopped locomoting at the ends of the maze arms to receive reward and also stopped intermittently elsewhere in the maze (Extended Data Fig. 1a). b, Spatial coverage in the hippocampal unit populations (mean ± s.e.m.; # of units: CA1: 476, CA2 P: 142, CA2 N: 79, CA3: 271). The CA2 N and P unit populations showed the lowest and highest spatial coverages, respectively (Kruskal-Wallis ANOVA, Tukey's post hoc tests, CA2 P > each other population, p = 0.0015; CA2 N < each other population, p < 10-6). Asterisks: **, p < 0.01; ***, p ≪ 0.001. c, Reward well firing of four example CA2 N units. Each column corresponds to a unit. For each well, the last ten visits (in a task recording epoch) are shown. Grey line: time of well entry (t = 0); yellow line: time of reward delivery (omitted in error trials). SWR periods are shown as pink zones. The two leftmost units were recorded simultaneously and on the same tetrode. d, Well specificity distribution in the N unit population. Mean ± s.e.m.: 0.78 ± 0.03 (n = 53 units).

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
N units signal current location during immobilitySpatial firing maps of five example CA2 site units. Each column corresponds to a unit. Upper row: positions visited (grey) and positions where the unit fired (colored points: P units in red, N units in blue). Total number of spikes is reported at upper right. Lower row: occupancy-normalized firing maps. Peak spatial firing rate is reported at upper right. Subjects stopped locomoting at the ends of the maze arms to receive reward and also stopped intermittently elsewhere in the maze (Extended Data Fig. 1a). b, Spatial coverage in the hippocampal unit populations (mean ± s.e.m.; # of units: CA1: 476, CA2 P: 142, CA2 N: 79, CA3: 271). The CA2 N and P unit populations showed the lowest and highest spatial coverages, respectively (Kruskal-Wallis ANOVA, Tukey's post hoc tests, CA2 P > each other population, p = 0.0015; CA2 N < each other population, p < 10-6). Asterisks: **, p < 0.01; ***, p ≪ 0.001. c, Reward well firing of four example CA2 N units. Each column corresponds to a unit. For each well, the last ten visits (in a task recording epoch) are shown. Grey line: time of well entry (t = 0); yellow line: time of reward delivery (omitted in error trials). SWR periods are shown as pink zones. The two leftmost units were recorded simultaneously and on the same tetrode. d, Well specificity distribution in the N unit population. Mean ± s.e.m.: 0.78 ± 0.03 (n = 53 units).
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Figure 13: N units signal current location during immobilitySpatial firing maps of five example CA2 site units. Each column corresponds to a unit. Upper row: positions visited (grey) and positions where the unit fired (colored points: P units in red, N units in blue). Total number of spikes is reported at upper right. Lower row: occupancy-normalized firing maps. Peak spatial firing rate is reported at upper right. Subjects stopped locomoting at the ends of the maze arms to receive reward and also stopped intermittently elsewhere in the maze (Extended Data Fig. 1a). b, Spatial coverage in the hippocampal unit populations (mean ± s.e.m.; # of units: CA1: 476, CA2 P: 142, CA2 N: 79, CA3: 271). The CA2 N and P unit populations showed the lowest and highest spatial coverages, respectively (Kruskal-Wallis ANOVA, Tukey's post hoc tests, CA2 P > each other population, p = 0.0015; CA2 N < each other population, p < 10-6). Asterisks: **, p < 0.01; ***, p ≪ 0.001. c, Reward well firing of four example CA2 N units. Each column corresponds to a unit. For each well, the last ten visits (in a task recording epoch) are shown. Grey line: time of well entry (t = 0); yellow line: time of reward delivery (omitted in error trials). SWR periods are shown as pink zones. The two leftmost units were recorded simultaneously and on the same tetrode. d, Well specificity distribution in the N unit population. Mean ± s.e.m.: 0.78 ± 0.03 (n = 53 units).
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