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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 fire more at low speeds and during immobilityFiring of four example CA2 N units during task behavior. Each row corresponds to an N unit, with spike rasters plotted above the traces. Left y-axis and grey fill trace: head speed (cm/s) of the subject. Right y-axis and blue fill trace: instantaneous firing rate (Hz). Right panels: spatial firing maps from corresponding task epochs. Grey: positions visited; colored points (darker color values at lower speeds): positions at which firing occurred, with each point opaque and plotted chronologically. b, Distribution of correlations (Pearson's r) between firing rate and log speed for each hippocampal unit population. Asterisks: ***, p ≪ 0.001 (vs. r = 0). c, Mean firing rates during task epochs (mean ± s.e.m.; # of units: CA1: 478, CA3: 271, CA2 P: 142, CA2 N: 84). Across unit populations, N units showed the highest firing rates during non-SWR immobility (Kruskal-Wallis ANOVA, Tukey's post hoc tests for CA2 N > each other population, p < 0.001). Moreover, N unit firing was higher during non-SWR immobility than during locomotion (p < 10-10, signed-rank) and also SWRs (p < 10-12, signed-rank). Asterisks: ***, p < 0.001 or p ≪ 0.001.
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Figure 12: N units fire more at low speeds and during immobilityFiring of four example CA2 N units during task behavior. Each row corresponds to an N unit, with spike rasters plotted above the traces. Left y-axis and grey fill trace: head speed (cm/s) of the subject. Right y-axis and blue fill trace: instantaneous firing rate (Hz). Right panels: spatial firing maps from corresponding task epochs. Grey: positions visited; colored points (darker color values at lower speeds): positions at which firing occurred, with each point opaque and plotted chronologically. b, Distribution of correlations (Pearson's r) between firing rate and log speed for each hippocampal unit population. Asterisks: ***, p ≪ 0.001 (vs. r = 0). c, Mean firing rates during task epochs (mean ± s.e.m.; # of units: CA1: 478, CA3: 271, CA2 P: 142, CA2 N: 84). Across unit populations, N units showed the highest firing rates during non-SWR immobility (Kruskal-Wallis ANOVA, Tukey's post hoc tests for CA2 N > each other population, p < 0.001). Moreover, N unit firing was higher during non-SWR immobility than during locomotion (p < 10-10, signed-rank) and also SWRs (p < 10-12, signed-rank). Asterisks: ***, p < 0.001 or p ≪ 0.001.

Mentions: We next examined the relationship of N unit firing to ongoing behavior. We found that N units fired mainly at low movement speeds and during immobility (Fig. 2a). To characterize this relationship, we first evaluated the correlation between unit firing rate and speed (Fig. 2b). The CA1 and CA3 unit populations both showed overall positive correlation, consistent with previous reports26-28 (Pearson r, firing rate vs. log speed; mean ± s.d.; CA1: 0.11 ± 0.10, CA1 vs. 0, p < 10-58, signed-rank; CA3: 0.06 ± 0.11, CA3 vs. 0, p < 10-14, signed-rank). Remarkably, the CA2 N and CA2 P unit populations showed dramatically different distributions: P units were positively correlated while N units were almost exclusively negatively correlated (mean ± s.d.; CA2 P: 0.10 ± 0.13, CA2 P vs. 0, p < 10-11, signed-rank; CA2 N: -0.10 ± 0.09, CA2 N vs. 0, p < 10-10, signed-rank; CA2 N vs. CA2 P, p < 10-19, rank-sum). N units also fired at higher rates than all other unit populations during immobility (Fig. 2c). These findings indicated a fundamental distinction between N units and classic hippocampal place cells.


A hippocampal network for spatial coding during immobility and sleep
N units fire more at low speeds and during immobilityFiring of four example CA2 N units during task behavior. Each row corresponds to an N unit, with spike rasters plotted above the traces. Left y-axis and grey fill trace: head speed (cm/s) of the subject. Right y-axis and blue fill trace: instantaneous firing rate (Hz). Right panels: spatial firing maps from corresponding task epochs. Grey: positions visited; colored points (darker color values at lower speeds): positions at which firing occurred, with each point opaque and plotted chronologically. b, Distribution of correlations (Pearson's r) between firing rate and log speed for each hippocampal unit population. Asterisks: ***, p ≪ 0.001 (vs. r = 0). c, Mean firing rates during task epochs (mean ± s.e.m.; # of units: CA1: 478, CA3: 271, CA2 P: 142, CA2 N: 84). Across unit populations, N units showed the highest firing rates during non-SWR immobility (Kruskal-Wallis ANOVA, Tukey's post hoc tests for CA2 N > each other population, p < 0.001). Moreover, N unit firing was higher during non-SWR immobility than during locomotion (p < 10-10, signed-rank) and also SWRs (p < 10-12, signed-rank). Asterisks: ***, p < 0.001 or p ≪ 0.001.
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Figure 12: N units fire more at low speeds and during immobilityFiring of four example CA2 N units during task behavior. Each row corresponds to an N unit, with spike rasters plotted above the traces. Left y-axis and grey fill trace: head speed (cm/s) of the subject. Right y-axis and blue fill trace: instantaneous firing rate (Hz). Right panels: spatial firing maps from corresponding task epochs. Grey: positions visited; colored points (darker color values at lower speeds): positions at which firing occurred, with each point opaque and plotted chronologically. b, Distribution of correlations (Pearson's r) between firing rate and log speed for each hippocampal unit population. Asterisks: ***, p ≪ 0.001 (vs. r = 0). c, Mean firing rates during task epochs (mean ± s.e.m.; # of units: CA1: 478, CA3: 271, CA2 P: 142, CA2 N: 84). Across unit populations, N units showed the highest firing rates during non-SWR immobility (Kruskal-Wallis ANOVA, Tukey's post hoc tests for CA2 N > each other population, p < 0.001). Moreover, N unit firing was higher during non-SWR immobility than during locomotion (p < 10-10, signed-rank) and also SWRs (p < 10-12, signed-rank). Asterisks: ***, p < 0.001 or p ≪ 0.001.
Mentions: We next examined the relationship of N unit firing to ongoing behavior. We found that N units fired mainly at low movement speeds and during immobility (Fig. 2a). To characterize this relationship, we first evaluated the correlation between unit firing rate and speed (Fig. 2b). The CA1 and CA3 unit populations both showed overall positive correlation, consistent with previous reports26-28 (Pearson r, firing rate vs. log speed; mean ± s.d.; CA1: 0.11 ± 0.10, CA1 vs. 0, p < 10-58, signed-rank; CA3: 0.06 ± 0.11, CA3 vs. 0, p < 10-14, signed-rank). Remarkably, the CA2 N and CA2 P unit populations showed dramatically different distributions: P units were positively correlated while N units were almost exclusively negatively correlated (mean ± s.d.; CA2 P: 0.10 ± 0.13, CA2 P vs. 0, p < 10-11, signed-rank; CA2 N: -0.10 ± 0.09, CA2 N vs. 0, p < 10-10, signed-rank; CA2 N vs. CA2 P, p < 10-19, rank-sum). N units also fired at higher rates than all other unit populations during immobility (Fig. 2c). These findings indicated a fundamental distinction between N units and classic hippocampal place cells.

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