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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.


Related in: MedlinePlus

N wave: a novel hippocampal network pattern at 1-4 Hza, Non-SWR immobility STAs of wide-band (0.5-400 Hz, upper section) and low frequency-band (1-4 Hz, lower section) filtered LFP. Plotted are mean STAs of hippocampal LFP for each principal unit population (first four columns). LFP from four distinct recording sites (REF, CA2, CA3, DG) are plotted in rows. The mean RTA (fifth column) was calculated from individual RTAs that were matched (same recording epochs) to each CA2 N unit, and thus have the same sample sizes as N units. Vertical lines correspond to the time of spiking (STAs) or SWRs (RTA). The width of the trace indicates ± s.e.m. over individual unit STAs or RTAs. The total trace length is 2 s. REF: reference electrode located in corpus callosum overlying dorsal hippocampus, reporting signals relative to a cerebellar ground screw. Scale bars: x: 250 ms, y: 50 μV. b, All CA2 N unit STAs for spiking during non-SWR immobility. 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). 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 (STAs) or SWRs (RTAs), with a dot indicating significance vs. 0 μV (p < 0.05, rank-sum). The STA of an unclassified unit (see Supplementary Methods) is indicated with an empty box. c, STA vs. matched RTA voltage amplitudes (1-4 Hz LFP measured at t = 0; STA: time of spike, RTA: time of peak ripple power) for individual CA2 N units (n = 58). CA2 N unit STA amplitudes (black circles) were larger than that of their matched RTAs (pink circles) (mean ± s.e.m., STA: 47 ± 6 μV, RTA: -168 ± 10 μV; p < 10-10, signed-rank) and also 0 μV (p < 10-7, signed-rank). Asterisks: ***, p ≪ 0.001. d, All interneuronal unit STAs for spiking during non-SWR immobility periods. Interneuronal units were analyzed for coupling to LFP since hippocampal interneurons show temporally precise firing relationships with all canonical hippocampal network patterns79. Seventy-eight putative interneuronal units were recorded in or near the cell layers of CA1, CA2, CA3, and DG; of these units, 63 were recorded when valid CA2, CA3, or DG LFP recordings were simultaneously available and reporting SWR sharp waves as negative transients. Of the 63 units, 27 fired in association with the N wave (criteria in Supplementary Methods; CA1: 10, CA2: 4, CA3: 7, and DG: 6). In the plot, 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). 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 indicated with an empty box. e, Mean firing rate of interneuronal units (mean ± s.e.m.) with negative (black; n = 36) vs. positive (orange; n = 27) STAs. f, Firing rate vs. speed correlation (Pearson's r) of interneuronal units with negative (black) vs. positive (orange) STAs. Task epochs were analyzed. g, Peri-SWR time histograms (PSTHs) of firing for interneuronal units with negative (left) and positive (right) STAs. Negative STA units uniformly exhibited a sharp peak in firing at the time of SWRs while positive STA units showed instances in which unit firing decreased from baseline levels (unit # 1-4, 6, 8) or showed an increase in firing that was less sharp (unit # 23-25)79-81.
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Figure 7: N wave: a novel hippocampal network pattern at 1-4 Hza, Non-SWR immobility STAs of wide-band (0.5-400 Hz, upper section) and low frequency-band (1-4 Hz, lower section) filtered LFP. Plotted are mean STAs of hippocampal LFP for each principal unit population (first four columns). LFP from four distinct recording sites (REF, CA2, CA3, DG) are plotted in rows. The mean RTA (fifth column) was calculated from individual RTAs that were matched (same recording epochs) to each CA2 N unit, and thus have the same sample sizes as N units. Vertical lines correspond to the time of spiking (STAs) or SWRs (RTA). The width of the trace indicates ± s.e.m. over individual unit STAs or RTAs. The total trace length is 2 s. REF: reference electrode located in corpus callosum overlying dorsal hippocampus, reporting signals relative to a cerebellar ground screw. Scale bars: x: 250 ms, y: 50 μV. b, All CA2 N unit STAs for spiking during non-SWR immobility. 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). 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 (STAs) or SWRs (RTAs), with a dot indicating significance vs. 0 μV (p < 0.05, rank-sum). The STA of an unclassified unit (see Supplementary Methods) is indicated with an empty box. c, STA vs. matched RTA voltage amplitudes (1-4 Hz LFP measured at t = 0; STA: time of spike, RTA: time of peak ripple power) for individual CA2 N units (n = 58). CA2 N unit STA amplitudes (black circles) were larger than that of their matched RTAs (pink circles) (mean ± s.e.m., STA: 47 ± 6 μV, RTA: -168 ± 10 μV; p < 10-10, signed-rank) and also 0 μV (p < 10-7, signed-rank). Asterisks: ***, p ≪ 0.001. d, All interneuronal unit STAs for spiking during non-SWR immobility periods. Interneuronal units were analyzed for coupling to LFP since hippocampal interneurons show temporally precise firing relationships with all canonical hippocampal network patterns79. Seventy-eight putative interneuronal units were recorded in or near the cell layers of CA1, CA2, CA3, and DG; of these units, 63 were recorded when valid CA2, CA3, or DG LFP recordings were simultaneously available and reporting SWR sharp waves as negative transients. Of the 63 units, 27 fired in association with the N wave (criteria in Supplementary Methods; CA1: 10, CA2: 4, CA3: 7, and DG: 6). In the plot, 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). 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 indicated with an empty box. e, Mean firing rate of interneuronal units (mean ± s.e.m.) with negative (black; n = 36) vs. positive (orange; n = 27) STAs. f, Firing rate vs. speed correlation (Pearson's r) of interneuronal units with negative (black) vs. positive (orange) STAs. Task epochs were analyzed. g, Peri-SWR time histograms (PSTHs) of firing for interneuronal units with negative (left) and positive (right) STAs. Negative STA units uniformly exhibited a sharp peak in firing at the time of SWRs while positive STA units showed instances in which unit firing decreased from baseline levels (unit # 1-4, 6, 8) or showed an increase in firing that was less sharp (unit # 23-25)79-81.

Mentions: In contrast to STAs from locomotor periods (characterized by the expected ∼8 Hz theta frequency modulation18,32, Extended Data Fig. 6), STAs from non-SWR immobility periods (Fig. 4b, c, Extended Data Fig. 7a) showed that N units fired at the time of a positive transient LFP pattern lasting ∼200 ms. The pattern was smallest on the parent electrode in CA2, larger in CA3, and largest at DG, suggesting broad engagement of the hippocampal circuit. Furthermore, unlike N units, P units showed a mean STA characterized by a negative transient similar to the canonical sharp wave transient of SWRs33 (Fig. 4b, c).


A hippocampal network for spatial coding during immobility and sleep
N wave: a novel hippocampal network pattern at 1-4 Hza, Non-SWR immobility STAs of wide-band (0.5-400 Hz, upper section) and low frequency-band (1-4 Hz, lower section) filtered LFP. Plotted are mean STAs of hippocampal LFP for each principal unit population (first four columns). LFP from four distinct recording sites (REF, CA2, CA3, DG) are plotted in rows. The mean RTA (fifth column) was calculated from individual RTAs that were matched (same recording epochs) to each CA2 N unit, and thus have the same sample sizes as N units. Vertical lines correspond to the time of spiking (STAs) or SWRs (RTA). The width of the trace indicates ± s.e.m. over individual unit STAs or RTAs. The total trace length is 2 s. REF: reference electrode located in corpus callosum overlying dorsal hippocampus, reporting signals relative to a cerebellar ground screw. Scale bars: x: 250 ms, y: 50 μV. b, All CA2 N unit STAs for spiking during non-SWR immobility. 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). 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 (STAs) or SWRs (RTAs), with a dot indicating significance vs. 0 μV (p < 0.05, rank-sum). The STA of an unclassified unit (see Supplementary Methods) is indicated with an empty box. c, STA vs. matched RTA voltage amplitudes (1-4 Hz LFP measured at t = 0; STA: time of spike, RTA: time of peak ripple power) for individual CA2 N units (n = 58). CA2 N unit STA amplitudes (black circles) were larger than that of their matched RTAs (pink circles) (mean ± s.e.m., STA: 47 ± 6 μV, RTA: -168 ± 10 μV; p < 10-10, signed-rank) and also 0 μV (p < 10-7, signed-rank). Asterisks: ***, p ≪ 0.001. d, All interneuronal unit STAs for spiking during non-SWR immobility periods. Interneuronal units were analyzed for coupling to LFP since hippocampal interneurons show temporally precise firing relationships with all canonical hippocampal network patterns79. Seventy-eight putative interneuronal units were recorded in or near the cell layers of CA1, CA2, CA3, and DG; of these units, 63 were recorded when valid CA2, CA3, or DG LFP recordings were simultaneously available and reporting SWR sharp waves as negative transients. Of the 63 units, 27 fired in association with the N wave (criteria in Supplementary Methods; CA1: 10, CA2: 4, CA3: 7, and DG: 6). In the plot, 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). 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 indicated with an empty box. e, Mean firing rate of interneuronal units (mean ± s.e.m.) with negative (black; n = 36) vs. positive (orange; n = 27) STAs. f, Firing rate vs. speed correlation (Pearson's r) of interneuronal units with negative (black) vs. positive (orange) STAs. Task epochs were analyzed. g, Peri-SWR time histograms (PSTHs) of firing for interneuronal units with negative (left) and positive (right) STAs. Negative STA units uniformly exhibited a sharp peak in firing at the time of SWRs while positive STA units showed instances in which unit firing decreased from baseline levels (unit # 1-4, 6, 8) or showed an increase in firing that was less sharp (unit # 23-25)79-81.
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Figure 7: N wave: a novel hippocampal network pattern at 1-4 Hza, Non-SWR immobility STAs of wide-band (0.5-400 Hz, upper section) and low frequency-band (1-4 Hz, lower section) filtered LFP. Plotted are mean STAs of hippocampal LFP for each principal unit population (first four columns). LFP from four distinct recording sites (REF, CA2, CA3, DG) are plotted in rows. The mean RTA (fifth column) was calculated from individual RTAs that were matched (same recording epochs) to each CA2 N unit, and thus have the same sample sizes as N units. Vertical lines correspond to the time of spiking (STAs) or SWRs (RTA). The width of the trace indicates ± s.e.m. over individual unit STAs or RTAs. The total trace length is 2 s. REF: reference electrode located in corpus callosum overlying dorsal hippocampus, reporting signals relative to a cerebellar ground screw. Scale bars: x: 250 ms, y: 50 μV. b, All CA2 N unit STAs for spiking during non-SWR immobility. 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). 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 (STAs) or SWRs (RTAs), with a dot indicating significance vs. 0 μV (p < 0.05, rank-sum). The STA of an unclassified unit (see Supplementary Methods) is indicated with an empty box. c, STA vs. matched RTA voltage amplitudes (1-4 Hz LFP measured at t = 0; STA: time of spike, RTA: time of peak ripple power) for individual CA2 N units (n = 58). CA2 N unit STA amplitudes (black circles) were larger than that of their matched RTAs (pink circles) (mean ± s.e.m., STA: 47 ± 6 μV, RTA: -168 ± 10 μV; p < 10-10, signed-rank) and also 0 μV (p < 10-7, signed-rank). Asterisks: ***, p ≪ 0.001. d, All interneuronal unit STAs for spiking during non-SWR immobility periods. Interneuronal units were analyzed for coupling to LFP since hippocampal interneurons show temporally precise firing relationships with all canonical hippocampal network patterns79. Seventy-eight putative interneuronal units were recorded in or near the cell layers of CA1, CA2, CA3, and DG; of these units, 63 were recorded when valid CA2, CA3, or DG LFP recordings were simultaneously available and reporting SWR sharp waves as negative transients. Of the 63 units, 27 fired in association with the N wave (criteria in Supplementary Methods; CA1: 10, CA2: 4, CA3: 7, and DG: 6). In the plot, 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). 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 indicated with an empty box. e, Mean firing rate of interneuronal units (mean ± s.e.m.) with negative (black; n = 36) vs. positive (orange; n = 27) STAs. f, Firing rate vs. speed correlation (Pearson's r) of interneuronal units with negative (black) vs. positive (orange) STAs. Task epochs were analyzed. g, Peri-SWR time histograms (PSTHs) of firing for interneuronal units with negative (left) and positive (right) STAs. Negative STA units uniformly exhibited a sharp peak in firing at the time of SWRs while positive STA units showed instances in which unit firing decreased from baseline levels (unit # 1-4, 6, 8) or showed an increase in firing that was less sharp (unit # 23-25)79-81.
Mentions: In contrast to STAs from locomotor periods (characterized by the expected ∼8 Hz theta frequency modulation18,32, Extended Data Fig. 6), STAs from non-SWR immobility periods (Fig. 4b, c, Extended Data Fig. 7a) showed that N units fired at the time of a positive transient LFP pattern lasting ∼200 ms. The pattern was smallest on the parent electrode in CA2, larger in CA3, and largest at DG, suggesting broad engagement of the hippocampal circuit. Furthermore, unlike N units, P units showed a mean STA characterized by a negative transient similar to the canonical sharp wave transient of SWRs33 (Fig. 4b, c).

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