To chart list... What is the role of sleep on hippocampus-dependent memory consolidation? - a
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Chart Owner: Alex Holcombe
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Hypotheses
Evidence
Passive Role
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Sleep transiently shelters memories from interference.
No Role
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Sleep contributes nothing to memory.
Permissive Role
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Sleep creates conditions conducive to memory consolidation (which can also occur during a waking period), but plays no special role in the consolidation process.
Active Role
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Consolidation process that is unique to sleep and does not occur outside of sleep.
Ebbinghaus (1885)/cite:Ebbinghaus1885NewYo-1
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The slope of forgetting was less steep after 24 hr. The 24 hr period always included sleep.
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Jenkins & Dallenbach (1924)/cite:JenkinsDallenbach1924Ameri
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Less forgetting of nonsense syllables after sleep period than after wake period. Suggests sleep may delay forgetting simply because no new competing information is encoded during sleep
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Graves et al. (2003)/cite:GravesHellerPackAbelGravesHellerPackAbelLearn
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Post-training sleep deprivation in rats impairs context fear memory but not cued fear memory.
Suggests that lack of sleep selectively impairs consolidation of hippocampus-dependent memories. Takes advantage of both hippocampus-dependent and -independent components of Pavlovian fear conditioning to dissociate the effect.
Cai et al. (2009)/cite:AnagnostarCaiHarrisonSageShuman2009Learn
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Gentle handling (part of the usual rodent sleep deprivation procedure) impairs consolidation, regardless of sleep.
Suggests that deficits found in prior sleep deprivation studies may have been a result of stress as opposed to the lack of sleep.
Gais et al. (2006)/cite:GaisLucasBornLearn
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Vocab words learned closer to a sleep period were more likely to be remembered. If sleep did not occur within 24 hr after learning, memory was impaired, even with recovery sleep. Circadian and homeostatic factors were controlled for.
Ellenbogen et al. (2006)
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Participants learned a list of paired associates (A-B). After a 12 hr retention interval that included either sleep or wakefulness, half of the participants were tested on A-B pairs (Sleep and Wake groups); the remaining participants learned an interfering list (A-C) 12 min prior to testing. The groups that had sleep performed better in the interference group than the one that did not have sleep. Sleep stabilized memory, making it more resistant to future interference.
Gais & Born (2004)/cite:GaisBornGaisBornLearn
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Subjects who slept the first half of night (mostly SWS and a state of low ACh) had better memory retention than those who slept the second half of the night (mostly REM sleep and a high state of ACh). Increasing ACh levels via physostigmine reduced the benefit of sleep on memory.
Plihal & Born (1997)/cite:PlihalBorn1999Psych
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Those sleeping the first half of the night (mostly SWS) did better on declarative memory (paired-associate task) than those that slept the second half of the night (mostly REM), who did better on a mirror-tracing task.
Wilson & McNaughton (1994)/cite:WilsonMcNaughton1994Scien
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Places cells that were active during "training" were reactivated during sleep.
Mechanistic evidence of consolidation during sleep. Place cells that were active during training were reactivated during the sleep period. Didn't check whether this also occurs during other periods, like quiet rest
Siapas & Wilson (1998)/cite:SiapasWilson1998Neuro
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Sharp waves & ripples in the hippocampus are temporally correlated with cortical spindles during SWS, suggesting hippocampal-cortex dialogue, one form of which is memory consolidation.
Karlsson & Frank (2009)/cite:FrankKarlsson2009NatNe
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Neural replay occurred for both waking and sleep. They found frequent awake replay of sequences of place cells from a previous experience. These results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay.
Marshall et al. (2004)/cite:MarshallMlleHallschmidBorn2004JNeur
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Induction of slow-wave activity in the frontal cortex via transcranial direct current stimulation improved memory retention.
Direct experimental evidence that sleep, specifically slow-wave activity during sleep, is important for declarative memory.
Avoids common confounds such as circadian, homeostatic and sleep deprivation differences.
Cai et al. (2009)/cite:AnagnostarCaiGormanSageShuman2009Behav
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Sleep enhances context but not cued fear if post-training sleep occurs within 24 hrs. It does not need to occur immediately after training.
Tucker et al. (2006)/cite:TuckerHirotaWamsleyLauChakladerFishbein2006Neuro
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Naps with NREM sleep benefited memory retention.
+1 Weakly Confirms
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Suggests sleep plays a role
didn't manipulate whether sleep occurred
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+1 Weakly Confirms
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Suggests sleeps plays a role, however, it cannot speak to how strong or active sleep is in memory consolidation.
didn't manipulate whether sleep occurred
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+1 Weakly Confirms
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Forgetting was slower after a night of sleep; sleep possibly slowed the forgetting.
didn't manipulate whether sleep occurred
9
-1 Weakly Opposes
4
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Suggests sleep might slow forgetting
Maybe the same change in slope would be observed after 24 hrs even if the person didn't sleep, indicating that the change in slope has nothing to do with sleep
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+3
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When compared to an equal duration of wake, sleep yields less forgetting. Does not speak to how sleep slows forgetting.
the sleep and wake period occurred at different times of day. Therefore, the difference might be due to the circadian cycle rather than sleep itself. Also, there were only two subjects. Furthermore, it would take much stronger evidence to suggest that sleep is doing something unique to sleep and does not occur during other brain states.
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+3
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When compared to an equal duration of wake, sleep yields less forgetting. Does not speak to how sleep slows forgetting.
the sleep and wake period occurred at different times of day. Therefore, the difference might be due to the circadian cycle rather than sleep itself. Also, there were only two subjects.
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+3
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When compared to an equal duration of wake, sleep yields less forgetting
the sleep and wake period occurred at different times of day. Therefore, the difference might be due to the circadian cycle rather than sleep itself. Also, there were only two subjects.
11
-2
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When compared to an equal duration of wake, sleep yields less forgetting
the sleep and wake period occurred at different times of day. Therefore, the difference might be due to the circadian cycle rather than sleep itself. Also, there were only two subjects.
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+2
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Moderately suggests there is some role of sleep, although it's unclear what that role is.
The rat sleep deprivation method itself (i.e. water carousel, flower-pot, or handling) may induce the deficits. Indeed, the effects are likely due to an effect like stress rather than lack of sleep.
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+2
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Moderately suggests there is some role of sleep, although it's unclear what that role is.
The rat sleep deprivation method itself (i.e. water carousel, flower-pot, or handling) may induce the deficits. Indeed, the effects are likely due to an effect like stress rather than lack of sleep.
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+2
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Moderately suggests there is some role of sleep, although it's unclear what that role is.
The rat sleep deprivation method itself (i.e. water carousel, flower-pot, or handling) may induce the deficits. Indeed, the effects are likely due to an effect like stress rather than lack of sleep.
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-2
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Suggests that when there is a lack of sleep, there's impaired memory, although this could be due to alternative reasons.
The rat sleep deprivation method itself (i.e. water carousel, flower-pot, or handling) may induce the deficits. Indeed, the effects are likely due to an effect like stress rather than lack of sleep. ADD CAI ET AL CITATION HERE?
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+0 No Impact
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While this shows that gentle handling impairs memory, it does not directly test whether sleep is important for memory.
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+0 No Impact
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While this shows that gentle handling impairs memory, it does not directly test whether sleep is important for memory.
8
+1 Weakly Confirms
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While this shows that gentle handling impairs memory, it does not directly test whether sleep is important for memory.
9
+0 No Impact
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While this shows that gentle handling impairs memory, it does not directly test whether sleep is important for memory.
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+3
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Sleep changes the slope of forgetting (i.e. less steep). However, it does not speak to whether this type of consolidation is specific to sleep or also occurs during other brain states.
They control for circadian confounds by using a sleep deprivation group. However, previous studies suggest that sleep deprivation has its own methodological confounds, such as stress-induced amnesia.
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-3
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If sleep were just a transient protector of memories, then the forgetting would continue at the same rate after sleep. Rather, sleep made memories more resistant to interference, which suggests that sleep is not just delaying the same slope of forgetting. Sleep changes the slope of forgetting (i.e. less steep).
They control for circadian confounds by using a sleep deprivation group. However, previous studies suggest that sleep deprivation has its own methodological confounds, such as stress-induced amnesia.
5
+3
0
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Sleep changes the slope of forgetting (i.e. less steep). However, it does not speak to whether this type of consolidation is specific to sleep or also occurs during other brain states.
They control for circadian confounds by using a sleep deprivation group. However, previous studies suggest that sleep deprivation has its own methodological confounds, such as stress-induced amnesia.
11
-4
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Sleep not only stops forgetting during the sleep period, but makes the memories more resistant to activity during the wake period following sleep.
They control for circadian confounds by using a sleep deprivation group. However, previous studies suggest that sleep deprivation has its own methodological confounds, such as stress-induced amnesia.
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-5 Strongly Opposes
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Strong evidence that sleep is stabilizing memories, making it more resistant to interference.

Interference was controlled experimentally.
There are not proper circadian controls as the awake group was trained and tested at different times than the sleep group. Additionally, the difference in the no-interference sleep and wake groups were only statistically trendy (i.e. p<.05).
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-5 Strongly Opposes
0
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Strong evidence that sleep is stabilizing memories, making it more resistant to interference and not temporarily stopping forgetting only during sleep.

Interference was controlled experimentally.
There are not proper circadian controls as the awake group was trained and tested at different times than the sleep group. Additionally, the difference in the no-interference sleep and wake groups were only statistically trendy (i.e. p<.05).
3
+4 Confirms
0
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Strong evidence that sleep is stabilizing memories, making it more resistant to interference and not temporarily stopping forgetting only during sleep.

Interference was controlled experimentally. However, this experiment does not speak to whether this consolidation mechanism is specific to sleep or other brain states.
There are not proper circadian controls as the awake group was trained and tested at different times than the sleep group. Additionally, the difference in the no-interference sleep and wake groups were only statistically trendy (i.e. p<.05).
12
+4 Confirms
0
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Strong evidence that sleep is stabilizing memories, making it more resistant to interference and not temporarily stopping forgetting only during sleep.

Interference was controlled experimentally. However, this experiment does not speak to whether this consolidation mechanism is specific to sleep or other brain states.
There are not proper circadian controls as the awake group was trained and tested at different times than the sleep group. Additionally, the difference in the no-interference sleep and wake groups were only statistically trendy (i.e. p<.05).
12
-5 Strongly Opposes
0
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Strongly suggests that sleep directly affects consolidation. They found that a specific stage of sleep was important (i.e. SWS, which is low in ACh). They manipulated levels of ACh with a drug and found that increasing ACh during SWS disrupts memory consolidation.

Suggest that low levels of ACh, which occurs during SWS is important for memory consolidation.
This study used a sleep deprivation group as the control, which is problematic. The stress of sleep deprivation could have impaired normal time-based consolidation.
3
+4 Confirms
0
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Strongly suggests that sleep directly affects consolidation. They found that a specific stage of sleep was important (i.e. SWS, which is low in ACh). They experimentally manipulated levels of ACh with a drug and found that increasing ACh during SWS disrupts memory consolidation.

Suggests that low levels of ACh, which occurs during SWS is important for memory consolidation. So sleep seems to be important for memory, but its also possible that this state occurs outside of sleep. such as pharmacologically inducing a state of low ACh.
This study used a sleep deprivation group as the control, which is problematic. The stress of sleep deprivation could have impaired normal time-based consolidation.
12
+5 Strongly Confirms
0
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Strongly suggests that sleep directly affects consolidation. They found that a specific stage of sleep was important (i.e. SWS, which is low in ACh). They experimentally manipulated levels of ACh with a drug and found that increasing ACh during SWS disrupts memory consolidation.

Suggests that low levels of ACh, which occurs during SWS is important for memory consolidation. This study strongly suggests that a specific stage of sleep is critical for memory consolidation (i.e. SWS) and is related to levels of ACh.
This study used a sleep deprivation group as the control, which is problematic. The stress of sleep deprivation could have impaired normal time-based consolidation.
13
-5 Strongly Opposes
0
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Strongly suggests that sleep directly affects consolidation. They found that a specific stage of sleep was important (i.e. SWS, which is low in ACh). They experimentally manipulated levels of ACh with a drug and found that increasing ACh during SWS disrupts memory consolidation.

Suggests that low levels of ACh, which occurs during SWS is important for memory consolidation.
This study used a sleep deprivation group as the control, which is problematic. The stress of sleep deprivation could have impaired normal time-based consolidation.
3
+4 Confirms
0
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Early sleep, rich with SWS, facilitates declarative memory consolidation. Although strong evidence that sleep is not just "sheltering memories," it does not show that other brain states, such as quiet rest or pharmacologically-induced states, do not do the same thing.
This study has sleep deprivation and circadian confounds.
12
+4 Confirms
0
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Early sleep, rich with SWS, facilitates declarative memory consolidation. Although strong evidence that sleep is not just "sheltering memories," it does not show that other brain states, such as quiet rest or pharmacologically-induced states, do not do the same thing.
This study has sleep deprivation and circadian confounds.
12
-5 Strongly Opposes
0
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Early sleep, rich with SWS, facilitates declarative memory consolidation.
This study has sleep deprivation and circadian confounds.
3
-5 Strongly Opposes
0
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Early sleep, rich with SWS, facilitates declarative memory consolidation.
This study has sleep deprivation and circadian confounds.
3
+2
0
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The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
10
+2
0
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The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
10
-2
0
+
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
6
-2
0
+
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
6
+5 Strongly Confirms
0
+
Suggests that memory formation is strengthened during sleep and not just temporarily halted during sleep. However, its possible this also occurs in other brain states.
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
13
+3
0
+
Suggests that memory formation is strengthened during sleep and not just temporarily halted during sleep. However, its possible this also occurs in other brain states.
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
11
-3
0
+
Suggests that memory formation is strengthened during sleep and not just temporarily halted during sleep.
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
5
-3
0
+
Suggests that memory formation is strengthened during sleep and not just temporarily halted during sleep.
The rodents are over trained on the tasks so their behavioral performance is at asymptote. Therefore, no relationship can be made between replay and behavior. Also, replay was not reliably detected until several weeks after training, so the replay may reflect a well engrained pattern that is epiphenomenal to memory.
5
+1 Weakly Confirms
0
+
Neural replay has been predominantly thought of as a sleep phenomena. This suggests that replay is present during both sleep and waking behavior. Thus, if replay is the mechanism for consolidation and replay occurs outside of sleep, then consolidation may not require sleep.
It is possible the replay that occurs during wake is reflecting a different process than the replay that occurs during SWS, which is time-compressed (i.e. faster than activation during awake). The replay during wake may be reflecting the animal's conscious remembering of the traversed path, while the faster replay during SWS may be reflecting the persistent reverberating loop that is hypothesized to occur during consolidation. It is also possible that replay may not be related to memory consolidation, as no behavioral correlates were observed.
9
+1 Weakly Confirms
0
+
Neural replay has been predominantly thought of as a sleep phenomena. This suggests that replay is present during both sleep and waking behavior. Thus, if replay is the mechanism for consolidation and replay occurs outside of sleep, then consolidation may not require sleep. Quiet rest and sleep and similar in replay, suggesting that it's more about a state of least interference.
It is possible the replay that occurs during wake is reflecting a different process than the replay that occurs during SWS, which is time-compressed (i.e. 4-10 times faster than activation during awake). The replay during wake may be reflecting the animal's conscious remembering of the traversed path, while the faster replay during SWS may be reflecting the persistent reverberating loop that is hypothesized to occur during consolidation. It is also possible that replay may not be related to memory consolidation, as no behavioral correlates were observed.
9
+2
0
+
Neural replay has been predominantly thought of as a sleep phenomena. This suggests that replay is present during both sleep and waking behavior. Thus, if replay is the mechanism for consolidation and replay occurs outside of sleep, then consolidation may not require sleep. Quiet rest and sleep and similar in replay, suggesting that it's more about a state of least interference. These data are consistent with the permissive role, as that hypothesis would predict that a brain state with little interference would facilitate replay.
It is possible the replay that occurs during wake is reflecting a different process than the replay that occurs during SWS, which is time-compressed (i.e. 4-10 times faster than activation during awake). The replay during wake may be reflecting the animal's conscious remembering of the traversed path, while the faster replay during SWS may be reflecting the persistent reverberating loop that is hypothesized to occur during consolidation. It is also possible that replay may not be related to memory consolidation, as no behavioral correlates were observed.
10
-3
0
+
Neural replay has been predominantly thought of as a sleep phenomena. This suggests that replay is present during both sleep and waking behavior. Thus, if replay is the mechanism for consolidation and replay occurs outside of sleep, then consolidation may not require sleep. Quiet rest and sleep and similar in replay, suggesting that it's more about a state of least interference. These data are consistent with the permissive role, as that hypothesis would predict that a brain state with little interference would facilitate replay. The active role would predict that replay would only occur during sleep and not awake, as found in this paper.
It is possible the replay that occurs during wake is reflecting a different process than the replay that occurs during SWS, which is time-compressed (i.e. 4-10 times faster than activation during awake). The replay during wake may be reflecting the animal's conscious remembering of the traversed path, while the faster replay during SWS may be reflecting the persistent reverberating loop that is hypothesized to occur during consolidation. It is also possible that replay may not be related to memory consolidation, as no behavioral correlates were observed.
5
+4 Confirms
0
+
Unclear whether SWA resulted in improvement because it is a state which has little interference (i.e. new encoding) or something more unique to sleep.
The electrical currents induced an artificial brain state that does not naturally occur. It may have also caused a chain of events, including activation or deactivation of other brain areas that may have lead to the effect. Lastly, the neural replay hypothesis requires hippocampus to also have SWA to see benefits which was not the case in this study.
12
+4 Confirms
0
+
Unclear whether SWA resulted in improvement because it is a state which has little interference (i.e. new encoding) or something more unique to sleep.
The electrical currents induced an artificial brain state that does not naturally occur. It may have also caused a chain of events, including activation or deactivation of other brain areas that may have lead to the effect. Lastly, the neural replay hypothesis requires hippocampus to also have SWA to see benefits which was not the case in this study.
12
-5 Strongly Opposes
0
+
The electrical currents induced an artificial brain state that does not naturally occur. It may have also caused a chain of events, including activation or deactivation of other brain areas that may have lead to the effect. Lastly, the neural replay hypothesis requires hippocampus to also have SWA to see benefits which was not the case in this study.
3
-5 Strongly Opposes
0
+
The electrical currents induced an artificial brain state that does not naturally occur. It may have also caused a chain of events, including activation or deactivation of other brain areas that may have lead to the effect. Lastly, the neural replay hypothesis requires hippocampus to also have SWA to see benefits which was not the case in this study.
3
+1 Weakly Confirms
0
+
While strongly suggests the sleep phase to enhance context memory. However, sleep is not required to protect the memory from forgetting in the first day, as sleep can occur 12 hours after training.

Also suggests there is little interference during the rodents' quiet wake phase, so there should be consolidation occurring, but that was not observed in the behavioral results.
This study did not measure physiological sleep with EEG. It is also possible that sleep is protecting the memories from interference.
9
-5 Strongly Opposes
0
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Direct evidence that the sleep period is important for context memory in rodents. Having a delay interval of a sleep phase after training boosts memory performance compared to a delay interval of an awake phase (i.e. quiet wake).
This study did not measure physiological sleep with EEG. It is also possible that sleep is protecting the memories from interference.
3
-5 Strongly Opposes
0
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Direct evidence that the sleep period is important for context memory in rodents. Having a delay interval of a sleep phase after training boosts memory performance compared to a delay interval of an awake phase (i.e. quiet wake).
This study did not measure physiological sleep with EEG. It is also possible that sleep is protecting the memories from interference.
3
+5 Strongly Confirms
0
+
Strongly suggest the sleep phase to enhance context memory. However, sleep is not required to protect the memory from forgetting in the first day, as sleep can occur 12 hours after training.

Also suggests that it is sleep, not quiescence, that is necessary for consolidation.
This study did not measure physiological sleep with EEG. It is also possible that sleep is protecting the memories from interference.
13
+3
0
+
Strong evidence that sleep is beneficial for declarative memory. They find that just having a bout of SWS improves memory retention compared to wake controls. By using a nap paradigm, they properly control for circadian and sleep deprivation issues.

However, because they do not compare different states of sleep, it cannot say the consolidation that occurred during sleep was specific to sleep as opposed to a lack of interference.
This study still has homeostatic factors, as nappers may have been more alert after a nap. Additionally, because the controls went on with their normal day, they could've had more interference impacting their memory. They needed a quiet rest control.
11
+3
0
+
Strong evidence that sleep is beneficial for declarative memory. They find that just having a bout of SWS improves memory retention compared to wake controls. By using a nap paradigm, they properly control for circadian and sleep deprivation issues.

However, because they do not compare different states of sleep, it cannot say the consolidation that occurred during sleep was specific to sleep as opposed to a lack of interference.
This study still has homeostatic factors, as nappers may have been more alert after a nap. Additionally, because the controls went on with their normal day, they could've had more interference impacting their memory. They needed a quiet rest control.
11
+0 No Impact
0
+
Strong evidence that sleep is beneficial for declarative memory. They find that just having a bout of SWS improves memory retention compared to wake controls. By using a nap paradigm, they properly control for circadian and sleep deprivation issues. However, because this study does not compare different states of sleep, it cannot say the consolidation that occurred during sleep was specific to sleep as opposed to a lack of interference.
This study still has homeostatic factors, as nappers may have been more alert after a nap. Additionally, because the controls went on with their normal day, they could've had more interference impacting their memory. They needed a quiet rest control.
8
-5 Strongly Opposes
0
+
Strong evidence that sleep is beneficial for declarative memory. They find that just having a bout of SWS improves memory retention compared to wake controls. By using a nap paradigm, they properly control for circadian and sleep deprivation issues.
This study still has homeostatic factors, as nappers may have been more alert after a nap. Additionally, because the controls went on with their normal day, they could've had more interference impacting their memory. They needed a quiet rest control.
3