Limits...
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 unit spatial codinga, Reward well firing rasters of 20 example N units. For each unit, data from the final ten (if available) entries of the subject's head into each of the three task reward wells (A, B, C) from a single task epoch are shown. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones. Note that firing for a given N unit was typically specific to one of the three reward wells. b, Non-reward well firing in three example N units. The rightmost example is the same as the third example in Fig. 2a. Upper row: spatial firing maps. Locations visited by the subject are plotted in grey, while locations at which the unit fired are plotted as colored opaque points (in blue) plotted chronologically and with darker color values at lower speeds. Total spike counts are indicated at upper right. In the task (Supplementary Methods and Extended Data Fig. 1a), reward was delivered to the subjects only at the ends of the maze arms, thus locations elsewhere in the maze were not directly associated with reward. Lower row: firing rate vs. speed of distinct visits to specific maze junctions (indicated with a square on spatial firing maps). Junction visits were identified as periods during which the subject's linear position (Supplementary Methods) was within 10 cm of a maze junction. Firing rate was the total number of spikes divided by the visit duration. Mean speed was the average instantaneous head speed during the visit. To limit analysis to discrete traversals through a junction, visits that were both less than 1 s in duration and also had mean speeds <10 cm/s were disregarded. Note that N units tended to fire at lower speed junction visits, and that some junction visits at higher speeds elicited no firing. c, Firing rate dependence on speed at non-reward task locations. Distribution of correlations (Pearson's r) between firing rate and log speed for each unit population. This analysis is the same as in Fig. 2b except restricted to periods when the subject was located >30 cm from reward wells, moreover including only units that fired at least 50 spikes outside of SWRs at these locations. As in the location-inclusive case (Fig. 2b), the N unit population uniquely showed an anti-correlation (r < 0) of firing rate with speed. Pearson's r, mean ± s.d.; CA1: 0.12 ± 0.20, CA1 vs. 0, p < 10-23, signed-rank; CA3: 0.11 ± 0.18, CA3 vs. 0, p < 10-13, signed-rank; CA2 P: 0.12 ± 0.16, CA2 P vs. 0, p < 10-10, signed-rank; CA2 N: -0.09 ± 0.20, CA2 N vs. 0, p = 0.0056, signed-rank; CA2 N vs. CA2 P, p < 10-8, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 386/393 units, CA3: 195/196 units, CA2 P: 121/121 units, CA2 N: 42/42 units). Asterisks: **, p < 0.01; ***, p < 0.001. d, Same analysis as c, except with an additional restriction to periods when the subject was located in positions where a unit had occupancy-normalized spatial coverage >2 Hz. Pearson's r, mean ± s.d.; CA1: 0.14 ± 0.30, CA1 vs. 0, p < 10-16, signed-rank; CA3: 0.17 ± 0.30, CA3 vs. 0, p < 10-10, signed-rank; CA2 P: 0.22 ± 0.23, CA2 P vs. 0, p < 10-12, signed-rank; CA2 N: -0.17 ± 0.33, CA2 N vs. 0, p = 0.031, signed-rank; CA2 N vs. CA2 P, p < 10-6, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 358/364 units, CA3: 168/168 units, CA2 P: 111/111 units, CA2 N: 23/24 units). Asterisks: *, p < 0.05; ***, p < 0.001.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC5037107&req=5

Figure 5: N unit spatial codinga, Reward well firing rasters of 20 example N units. For each unit, data from the final ten (if available) entries of the subject's head into each of the three task reward wells (A, B, C) from a single task epoch are shown. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones. Note that firing for a given N unit was typically specific to one of the three reward wells. b, Non-reward well firing in three example N units. The rightmost example is the same as the third example in Fig. 2a. Upper row: spatial firing maps. Locations visited by the subject are plotted in grey, while locations at which the unit fired are plotted as colored opaque points (in blue) plotted chronologically and with darker color values at lower speeds. Total spike counts are indicated at upper right. In the task (Supplementary Methods and Extended Data Fig. 1a), reward was delivered to the subjects only at the ends of the maze arms, thus locations elsewhere in the maze were not directly associated with reward. Lower row: firing rate vs. speed of distinct visits to specific maze junctions (indicated with a square on spatial firing maps). Junction visits were identified as periods during which the subject's linear position (Supplementary Methods) was within 10 cm of a maze junction. Firing rate was the total number of spikes divided by the visit duration. Mean speed was the average instantaneous head speed during the visit. To limit analysis to discrete traversals through a junction, visits that were both less than 1 s in duration and also had mean speeds <10 cm/s were disregarded. Note that N units tended to fire at lower speed junction visits, and that some junction visits at higher speeds elicited no firing. c, Firing rate dependence on speed at non-reward task locations. Distribution of correlations (Pearson's r) between firing rate and log speed for each unit population. This analysis is the same as in Fig. 2b except restricted to periods when the subject was located >30 cm from reward wells, moreover including only units that fired at least 50 spikes outside of SWRs at these locations. As in the location-inclusive case (Fig. 2b), the N unit population uniquely showed an anti-correlation (r < 0) of firing rate with speed. Pearson's r, mean ± s.d.; CA1: 0.12 ± 0.20, CA1 vs. 0, p < 10-23, signed-rank; CA3: 0.11 ± 0.18, CA3 vs. 0, p < 10-13, signed-rank; CA2 P: 0.12 ± 0.16, CA2 P vs. 0, p < 10-10, signed-rank; CA2 N: -0.09 ± 0.20, CA2 N vs. 0, p = 0.0056, signed-rank; CA2 N vs. CA2 P, p < 10-8, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 386/393 units, CA3: 195/196 units, CA2 P: 121/121 units, CA2 N: 42/42 units). Asterisks: **, p < 0.01; ***, p < 0.001. d, Same analysis as c, except with an additional restriction to periods when the subject was located in positions where a unit had occupancy-normalized spatial coverage >2 Hz. Pearson's r, mean ± s.d.; CA1: 0.14 ± 0.30, CA1 vs. 0, p < 10-16, signed-rank; CA3: 0.17 ± 0.30, CA3 vs. 0, p < 10-10, signed-rank; CA2 P: 0.22 ± 0.23, CA2 P vs. 0, p < 10-12, signed-rank; CA2 N: -0.17 ± 0.33, CA2 N vs. 0, p = 0.031, signed-rank; CA2 N vs. CA2 P, p < 10-6, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 358/364 units, CA3: 168/168 units, CA2 P: 111/111 units, CA2 N: 23/24 units). Asterisks: *, p < 0.05; ***, p < 0.001.

Mentions: In conjunction with low spatial coverage, N unit firing maps showed concentrated firing at locations where subjects were immobile (Fig. 3a, Extended Data Fig. 4c). To quantify possible spatial specificity in firing during immobility, we focused on firing at the maze reward wells since immobility at these locations was common across all subjects. Our analysis revealed that individual N units characteristically fired at specific single reward wells while remaining silent at the others (Fig. 3c, d, Extended Data Fig. 5a). Importantly, the location of N unit firing did not require direct association with reward since spatially specific firing was also observed at other maze locations (Extended Data Fig. 5b-d; seen previously in Fig. 2a, Fig. 3a, Extended Data Fig. 4c). These findings indicate that N unit firing constitutes a precise neural code for location during immobility.


A hippocampal network for spatial coding during immobility and sleep
N unit spatial codinga, Reward well firing rasters of 20 example N units. For each unit, data from the final ten (if available) entries of the subject's head into each of the three task reward wells (A, B, C) from a single task epoch are shown. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones. Note that firing for a given N unit was typically specific to one of the three reward wells. b, Non-reward well firing in three example N units. The rightmost example is the same as the third example in Fig. 2a. Upper row: spatial firing maps. Locations visited by the subject are plotted in grey, while locations at which the unit fired are plotted as colored opaque points (in blue) plotted chronologically and with darker color values at lower speeds. Total spike counts are indicated at upper right. In the task (Supplementary Methods and Extended Data Fig. 1a), reward was delivered to the subjects only at the ends of the maze arms, thus locations elsewhere in the maze were not directly associated with reward. Lower row: firing rate vs. speed of distinct visits to specific maze junctions (indicated with a square on spatial firing maps). Junction visits were identified as periods during which the subject's linear position (Supplementary Methods) was within 10 cm of a maze junction. Firing rate was the total number of spikes divided by the visit duration. Mean speed was the average instantaneous head speed during the visit. To limit analysis to discrete traversals through a junction, visits that were both less than 1 s in duration and also had mean speeds <10 cm/s were disregarded. Note that N units tended to fire at lower speed junction visits, and that some junction visits at higher speeds elicited no firing. c, Firing rate dependence on speed at non-reward task locations. Distribution of correlations (Pearson's r) between firing rate and log speed for each unit population. This analysis is the same as in Fig. 2b except restricted to periods when the subject was located >30 cm from reward wells, moreover including only units that fired at least 50 spikes outside of SWRs at these locations. As in the location-inclusive case (Fig. 2b), the N unit population uniquely showed an anti-correlation (r < 0) of firing rate with speed. Pearson's r, mean ± s.d.; CA1: 0.12 ± 0.20, CA1 vs. 0, p < 10-23, signed-rank; CA3: 0.11 ± 0.18, CA3 vs. 0, p < 10-13, signed-rank; CA2 P: 0.12 ± 0.16, CA2 P vs. 0, p < 10-10, signed-rank; CA2 N: -0.09 ± 0.20, CA2 N vs. 0, p = 0.0056, signed-rank; CA2 N vs. CA2 P, p < 10-8, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 386/393 units, CA3: 195/196 units, CA2 P: 121/121 units, CA2 N: 42/42 units). Asterisks: **, p < 0.01; ***, p < 0.001. d, Same analysis as c, except with an additional restriction to periods when the subject was located in positions where a unit had occupancy-normalized spatial coverage >2 Hz. Pearson's r, mean ± s.d.; CA1: 0.14 ± 0.30, CA1 vs. 0, p < 10-16, signed-rank; CA3: 0.17 ± 0.30, CA3 vs. 0, p < 10-10, signed-rank; CA2 P: 0.22 ± 0.23, CA2 P vs. 0, p < 10-12, signed-rank; CA2 N: -0.17 ± 0.33, CA2 N vs. 0, p = 0.031, signed-rank; CA2 N vs. CA2 P, p < 10-6, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 358/364 units, CA3: 168/168 units, CA2 P: 111/111 units, CA2 N: 23/24 units). Asterisks: *, p < 0.05; ***, p < 0.001.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC5037107&req=5

Figure 5: N unit spatial codinga, Reward well firing rasters of 20 example N units. For each unit, data from the final ten (if available) entries of the subject's head into each of the three task reward wells (A, B, C) from a single task epoch are shown. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones. Note that firing for a given N unit was typically specific to one of the three reward wells. b, Non-reward well firing in three example N units. The rightmost example is the same as the third example in Fig. 2a. Upper row: spatial firing maps. Locations visited by the subject are plotted in grey, while locations at which the unit fired are plotted as colored opaque points (in blue) plotted chronologically and with darker color values at lower speeds. Total spike counts are indicated at upper right. In the task (Supplementary Methods and Extended Data Fig. 1a), reward was delivered to the subjects only at the ends of the maze arms, thus locations elsewhere in the maze were not directly associated with reward. Lower row: firing rate vs. speed of distinct visits to specific maze junctions (indicated with a square on spatial firing maps). Junction visits were identified as periods during which the subject's linear position (Supplementary Methods) was within 10 cm of a maze junction. Firing rate was the total number of spikes divided by the visit duration. Mean speed was the average instantaneous head speed during the visit. To limit analysis to discrete traversals through a junction, visits that were both less than 1 s in duration and also had mean speeds <10 cm/s were disregarded. Note that N units tended to fire at lower speed junction visits, and that some junction visits at higher speeds elicited no firing. c, Firing rate dependence on speed at non-reward task locations. Distribution of correlations (Pearson's r) between firing rate and log speed for each unit population. This analysis is the same as in Fig. 2b except restricted to periods when the subject was located >30 cm from reward wells, moreover including only units that fired at least 50 spikes outside of SWRs at these locations. As in the location-inclusive case (Fig. 2b), the N unit population uniquely showed an anti-correlation (r < 0) of firing rate with speed. Pearson's r, mean ± s.d.; CA1: 0.12 ± 0.20, CA1 vs. 0, p < 10-23, signed-rank; CA3: 0.11 ± 0.18, CA3 vs. 0, p < 10-13, signed-rank; CA2 P: 0.12 ± 0.16, CA2 P vs. 0, p < 10-10, signed-rank; CA2 N: -0.09 ± 0.20, CA2 N vs. 0, p = 0.0056, signed-rank; CA2 N vs. CA2 P, p < 10-8, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 386/393 units, CA3: 195/196 units, CA2 P: 121/121 units, CA2 N: 42/42 units). Asterisks: **, p < 0.01; ***, p < 0.001. d, Same analysis as c, except with an additional restriction to periods when the subject was located in positions where a unit had occupancy-normalized spatial coverage >2 Hz. Pearson's r, mean ± s.d.; CA1: 0.14 ± 0.30, CA1 vs. 0, p < 10-16, signed-rank; CA3: 0.17 ± 0.30, CA3 vs. 0, p < 10-10, signed-rank; CA2 P: 0.22 ± 0.23, CA2 P vs. 0, p < 10-12, signed-rank; CA2 N: -0.17 ± 0.33, CA2 N vs. 0, p = 0.031, signed-rank; CA2 N vs. CA2 P, p < 10-6, rank-sum. Only units with significant correlations (p < 0.05) were included (CA1: 358/364 units, CA3: 168/168 units, CA2 P: 111/111 units, CA2 N: 23/24 units). Asterisks: *, p < 0.05; ***, p < 0.001.
Mentions: In conjunction with low spatial coverage, N unit firing maps showed concentrated firing at locations where subjects were immobile (Fig. 3a, Extended Data Fig. 4c). To quantify possible spatial specificity in firing during immobility, we focused on firing at the maze reward wells since immobility at these locations was common across all subjects. Our analysis revealed that individual N units characteristically fired at specific single reward wells while remaining silent at the others (Fig. 3c, d, Extended Data Fig. 5a). Importantly, the location of N unit firing did not require direct association with reward since spatially specific firing was also observed at other maze locations (Extended Data Fig. 5b-d; seen previously in Fig. 2a, Fig. 3a, Extended Data Fig. 4c). These findings indicate that N unit firing constitutes a precise neural code for location during immobility.

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