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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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CA1 and CA3 principal neurons fire in association with the N waveUnits showing positive STAs for spiking during non-SWR immobility periods were identified as firing in association with the N wave. a, All CA1 and CA3 principal unit STAs for spiking during non-SWR immobility periods. Only units with >100 spikes during these periods were analyzed. Unit STAs are grouped by polarity at the time of spiking (t = 0) and sorted by the time of the extremum (peak for positive; trough for negative) nearest the time of spiking. For each unit, LFP (1-4 Hz) from CA2, CA3, or DG (in increasing order of preference when available) was used. Colors indicate voltage (color bar at upper right). STAs are plotted on the left, while RTAs are plotted on the right. The center bar indicates the voltage polarity of the STA (orange: positive, black: negative) at the time of spiking (t = 0), with a dot indicating significance vs. 0 μV (p < 0.05, signed-rank). Unit STAs left unclassified (see Supplementary Methods) are plotted at bottom and indicated with an empty box. b, Firing rates for STA-classified unit populations during task epochs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). In both CA1 and CA3, units with positive STAs showed higher firing rates during non-SWR immobility (CA1 positive vs. CA1 negative, p < 10-9, rank-sum; CA3 positive vs. CA3 negative, p < 10-5, rank-sum), similar to CA2 N units (Fig. 2c). c, Spatial coverage in CA1 and CA3 units with negative vs. positive STAs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). CA1 units with positive STAs showed somewhat lower spatial coverage than units with negative STAs (CA1 negative vs. CA1 positive, p = 0.046, rank-sum), while an analogous difference in CA3 was not statistically significant (CA3 negative vs. CA3 positive, p = 0.12, rank-sum). d, Well specificity distributions in CA1 and CA3 units that had STA amplitudes (at time of spiking) significantly different from 0 μV (the units marked as significant in a and with available well data). For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.66 ± 0.04, CA1 positive: 0.86 ± 0.03; CA1 negative vs. CA1 positive, p < 10-4, rank-sum; CA3 negative: 0.49 ± 0.04, CA3 positive: 0.79 ± 0.04, CA3 negative vs. CA3 positive, p < 10-4, rank-sum). e, Well specificity distributions in CA1 and CA3 units with theta power cutoff. For each task epoch, the distribution of power in the theta band (5-11 Hz), averaged over CA1 recording sites, was calculated for immobility non-SWR periods. Spikes occurring during times in which the theta band power was in the upper quartile of this distribution were then excluded from well specificity calculations. For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.73 ± 0.05, CA1 positive: 0.87 ± 0.04; CA1 positive vs. CA1 negative, p < 0.002, rank-sum; CA3 negative: 0.58 ± 0.04, CA3 positive: 0.80 ± 0.04; CA3 negative vs. CA3 positive, p < 0.004, rank-sum).
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Figure 8: CA1 and CA3 principal neurons fire in association with the N waveUnits showing positive STAs for spiking during non-SWR immobility periods were identified as firing in association with the N wave. a, All CA1 and CA3 principal unit STAs for spiking during non-SWR immobility periods. Only units with >100 spikes during these periods were analyzed. Unit STAs are grouped by polarity at the time of spiking (t = 0) and sorted by the time of the extremum (peak for positive; trough for negative) nearest the time of spiking. For each unit, LFP (1-4 Hz) from CA2, CA3, or DG (in increasing order of preference when available) was used. Colors indicate voltage (color bar at upper right). STAs are plotted on the left, while RTAs are plotted on the right. The center bar indicates the voltage polarity of the STA (orange: positive, black: negative) at the time of spiking (t = 0), with a dot indicating significance vs. 0 μV (p < 0.05, signed-rank). Unit STAs left unclassified (see Supplementary Methods) are plotted at bottom and indicated with an empty box. b, Firing rates for STA-classified unit populations during task epochs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). In both CA1 and CA3, units with positive STAs showed higher firing rates during non-SWR immobility (CA1 positive vs. CA1 negative, p < 10-9, rank-sum; CA3 positive vs. CA3 negative, p < 10-5, rank-sum), similar to CA2 N units (Fig. 2c). c, Spatial coverage in CA1 and CA3 units with negative vs. positive STAs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). CA1 units with positive STAs showed somewhat lower spatial coverage than units with negative STAs (CA1 negative vs. CA1 positive, p = 0.046, rank-sum), while an analogous difference in CA3 was not statistically significant (CA3 negative vs. CA3 positive, p = 0.12, rank-sum). d, Well specificity distributions in CA1 and CA3 units that had STA amplitudes (at time of spiking) significantly different from 0 μV (the units marked as significant in a and with available well data). For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.66 ± 0.04, CA1 positive: 0.86 ± 0.03; CA1 negative vs. CA1 positive, p < 10-4, rank-sum; CA3 negative: 0.49 ± 0.04, CA3 positive: 0.79 ± 0.04, CA3 negative vs. CA3 positive, p < 10-4, rank-sum). e, Well specificity distributions in CA1 and CA3 units with theta power cutoff. For each task epoch, the distribution of power in the theta band (5-11 Hz), averaged over CA1 recording sites, was calculated for immobility non-SWR periods. Spikes occurring during times in which the theta band power was in the upper quartile of this distribution were then excluded from well specificity calculations. For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.73 ± 0.05, CA1 positive: 0.87 ± 0.04; CA1 positive vs. CA1 negative, p < 0.002, rank-sum; CA3 negative: 0.58 ± 0.04, CA3 positive: 0.80 ± 0.04; CA3 negative vs. CA3 positive, p < 0.004, rank-sum).

Mentions: We then asked whether neurons outside of CA2 were also N wave-coupled. We identified N wave-coupled units in CA1, CA3, and DG (Fig. 4e-i, Extended Data Figs. 7d-g, 8, 9), indicating that the N wave reflects a hippocampus-wide network pattern. Critically, a distinct subset of principal units was N wave-coupled (CA1: 50 units, CA3: 34 units, Fig. 4g-i, Extended Data Figs. 8, 9). As with CA2 N units, these units fired more during immobility than during movement (Extended Data Fig. 8b) and showed unequivocal location-specific firing during immobility (Fig. 4g, i and Extended Data Figs. 8d, e, 9), thereby linking the N wave network pattern to spatial coding during immobility across the hippocampus.


A hippocampal network for spatial coding during immobility and sleep
CA1 and CA3 principal neurons fire in association with the N waveUnits showing positive STAs for spiking during non-SWR immobility periods were identified as firing in association with the N wave. a, All CA1 and CA3 principal unit STAs for spiking during non-SWR immobility periods. Only units with >100 spikes during these periods were analyzed. Unit STAs are grouped by polarity at the time of spiking (t = 0) and sorted by the time of the extremum (peak for positive; trough for negative) nearest the time of spiking. For each unit, LFP (1-4 Hz) from CA2, CA3, or DG (in increasing order of preference when available) was used. Colors indicate voltage (color bar at upper right). STAs are plotted on the left, while RTAs are plotted on the right. The center bar indicates the voltage polarity of the STA (orange: positive, black: negative) at the time of spiking (t = 0), with a dot indicating significance vs. 0 μV (p < 0.05, signed-rank). Unit STAs left unclassified (see Supplementary Methods) are plotted at bottom and indicated with an empty box. b, Firing rates for STA-classified unit populations during task epochs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). In both CA1 and CA3, units with positive STAs showed higher firing rates during non-SWR immobility (CA1 positive vs. CA1 negative, p < 10-9, rank-sum; CA3 positive vs. CA3 negative, p < 10-5, rank-sum), similar to CA2 N units (Fig. 2c). c, Spatial coverage in CA1 and CA3 units with negative vs. positive STAs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). CA1 units with positive STAs showed somewhat lower spatial coverage than units with negative STAs (CA1 negative vs. CA1 positive, p = 0.046, rank-sum), while an analogous difference in CA3 was not statistically significant (CA3 negative vs. CA3 positive, p = 0.12, rank-sum). d, Well specificity distributions in CA1 and CA3 units that had STA amplitudes (at time of spiking) significantly different from 0 μV (the units marked as significant in a and with available well data). For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.66 ± 0.04, CA1 positive: 0.86 ± 0.03; CA1 negative vs. CA1 positive, p < 10-4, rank-sum; CA3 negative: 0.49 ± 0.04, CA3 positive: 0.79 ± 0.04, CA3 negative vs. CA3 positive, p < 10-4, rank-sum). e, Well specificity distributions in CA1 and CA3 units with theta power cutoff. For each task epoch, the distribution of power in the theta band (5-11 Hz), averaged over CA1 recording sites, was calculated for immobility non-SWR periods. Spikes occurring during times in which the theta band power was in the upper quartile of this distribution were then excluded from well specificity calculations. For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.73 ± 0.05, CA1 positive: 0.87 ± 0.04; CA1 positive vs. CA1 negative, p < 0.002, rank-sum; CA3 negative: 0.58 ± 0.04, CA3 positive: 0.80 ± 0.04; CA3 negative vs. CA3 positive, p < 0.004, rank-sum).
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Figure 8: CA1 and CA3 principal neurons fire in association with the N waveUnits showing positive STAs for spiking during non-SWR immobility periods were identified as firing in association with the N wave. a, All CA1 and CA3 principal unit STAs for spiking during non-SWR immobility periods. Only units with >100 spikes during these periods were analyzed. Unit STAs are grouped by polarity at the time of spiking (t = 0) and sorted by the time of the extremum (peak for positive; trough for negative) nearest the time of spiking. For each unit, LFP (1-4 Hz) from CA2, CA3, or DG (in increasing order of preference when available) was used. Colors indicate voltage (color bar at upper right). STAs are plotted on the left, while RTAs are plotted on the right. The center bar indicates the voltage polarity of the STA (orange: positive, black: negative) at the time of spiking (t = 0), with a dot indicating significance vs. 0 μV (p < 0.05, signed-rank). Unit STAs left unclassified (see Supplementary Methods) are plotted at bottom and indicated with an empty box. b, Firing rates for STA-classified unit populations during task epochs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). In both CA1 and CA3, units with positive STAs showed higher firing rates during non-SWR immobility (CA1 positive vs. CA1 negative, p < 10-9, rank-sum; CA3 positive vs. CA3 negative, p < 10-5, rank-sum), similar to CA2 N units (Fig. 2c). c, Spatial coverage in CA1 and CA3 units with negative vs. positive STAs (mean ± s.e.m.; # of units: CA1 negative: 86, CA1 positive: 50, CA3 negative: 100, CA3 positive: 34). CA1 units with positive STAs showed somewhat lower spatial coverage than units with negative STAs (CA1 negative vs. CA1 positive, p = 0.046, rank-sum), while an analogous difference in CA3 was not statistically significant (CA3 negative vs. CA3 positive, p = 0.12, rank-sum). d, Well specificity distributions in CA1 and CA3 units that had STA amplitudes (at time of spiking) significantly different from 0 μV (the units marked as significant in a and with available well data). For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.66 ± 0.04, CA1 positive: 0.86 ± 0.03; CA1 negative vs. CA1 positive, p < 10-4, rank-sum; CA3 negative: 0.49 ± 0.04, CA3 positive: 0.79 ± 0.04, CA3 negative vs. CA3 positive, p < 10-4, rank-sum). e, Well specificity distributions in CA1 and CA3 units with theta power cutoff. For each task epoch, the distribution of power in the theta band (5-11 Hz), averaged over CA1 recording sites, was calculated for immobility non-SWR periods. Spikes occurring during times in which the theta band power was in the upper quartile of this distribution were then excluded from well specificity calculations. For both CA1 and CA3, units with positive STAs showed higher well specificity (mean ± s.e.m., CA1 negative: 0.73 ± 0.05, CA1 positive: 0.87 ± 0.04; CA1 positive vs. CA1 negative, p < 0.002, rank-sum; CA3 negative: 0.58 ± 0.04, CA3 positive: 0.80 ± 0.04; CA3 negative vs. CA3 positive, p < 0.004, rank-sum).
Mentions: We then asked whether neurons outside of CA2 were also N wave-coupled. We identified N wave-coupled units in CA1, CA3, and DG (Fig. 4e-i, Extended Data Figs. 7d-g, 8, 9), indicating that the N wave reflects a hippocampus-wide network pattern. Critically, a distinct subset of principal units was N wave-coupled (CA1: 50 units, CA3: 34 units, Fig. 4g-i, Extended Data Figs. 8, 9). As with CA2 N units, these units fired more during immobility than during movement (Extended Data Fig. 8b) and showed unequivocal location-specific firing during immobility (Fig. 4g, i and Extended Data Figs. 8d, e, 9), thereby linking the N wave network pattern to spatial coding during immobility across the hippocampus.

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