During the Learning phase, the decrease in time spent exploring the same juvenile across the three sampling sessions served to confirm that the adult rat learned to discriminate the conspecific. The learning criterion was introduced to reduce variance in the behavioral expression of memory. Total exploration time spent with the juvenile rats was also analyzed. Statistical comparisons concentrated on: i cumulative scores for s intervals across the initial 3-min interval of the Test phase and, to assess slower dynamics; on ii cumulative scores for 1-min intervals across the entire min Test phase Note, for calculating cumulative scores, rather than the preference scores per se , only the time the animal spent with the novel and familiar juveniles, respectively, was cumulated for a given time interval.
Latency to explore the novel and familiar rat was analyzed with reference to the start of the Test session. To assess spatial memory , the exploration preference for the novel rat during the Test phase was calculated separately for four spatial sub-conditions depending on the retention conditions Sleep and Wake and the location of the novel juvenile rat with reference to the location of the familiar juvenile on the last i. Post hoc t -tests were used to specify significant main and interaction effects. All statistical analyses were performed using SPSS Estimates of effect size, i.
Another rat was excluded due to technical problem during the Test phase. In the Test phase, only rats of the Sleep group, but not of the Wake group, displayed significant social recognition memory as shown by preferential exploration of the novel juvenile conspecific. Analysis of s intervals revealed that sleep most profoundly affected exploration in the beginning of the Test phase. To assess slower changes, we cumulated exploration preference scores across subsequent 1-min intervals.
Figure 2. C Latency first approach to explore the novel rat and the familiar rat. D Total time spent exploring the juvenile rats novel and familiar cumulated across the first 3 min E and across the entiremin Test phase. There was no significant difference in total exploration time between groups. Latency to exploration of the familiar rat was significantly longer in the Sleep To discriminate interactions between the effects of sleep on social recognition and on spatial learning, exploration preferences in the Sleep and Wake groups were compared depending on whether the juvenile rat was located on the same spatial location Sleep-Same, Wake-Same groups or on a location different from that where the familiar rat was encountered in the last sampling session Sleep-Different, Wake-Different groups.
Separate analyses of the two spatial conditions revealed exploration scores that were above chance level, only in the Sleep-Different group, whereas in the other three conditions, i. In the Sleep-Different rats cumulated exploration scores reached significance during the first s interval and again towards the end of the 3-min period of analysis. Considering that exploration scores remained at chance level in three of the four conditions, we used planned contrasts to directly test the hypothesis that sleep specifically enhances social recognition depending on where the novel juvenile was placed.
Moreover, in the Sleep-Different group latency to explore the novel juvenile the first time was significantly shorter than that for the familiar juvenile Overall, these data indicate that sleep robustly enhances exploration towards the novel conspecific depending on where this novel rat is encountered, i. Figure 3. Note, only the Sleep-Different group shows above chance exploration preference in the first minute of the Test phase which also significantly differs from that of the Sleep-Same and Wake-Same groups and from that of the Wake-Different group during the first s interval, not shown.
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At the end of the Test phase, the exploration pattern in the Sleep groups reverses with higher exploration scores in the Sleep-Same than Sleep-Different group. Note, only the Sleep-Different group shows shorter latency to explore the novel rat in comparison to the familiar rat.
We examined the effect of post-learning sleep on consolidation of social recognition memory in rats. We found that sleep enhanced recognition of a conspecific as indicated by preferential exploration of the novel as compared to the familiar conspecific during the first min of the min Test phase. We also found clues that enhanced consolidation of social recognition memory during sleep depends on spatial context features of the social episode encoded before sleep: only the rats of the Sleep group which encountered the novel conspecific at a place different from that of the familiar rat during the last sampling phase, i.
This pattern of findings argues against a direct enhancing effect of sleep on social memory representations but is rather consistent with the notion that the consolidation effects of sleep on social and spatial aspects of a memory representation interact.
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While there is evidence that sleep in rats can facilitate intermediate and long-term memory for social information like the transmission of food preference Wooden et al. Against this backdrop the present study provides first time evidence that the memory of conspecifics can last distinctly longer after sleep, i. The sleep effect expressed itself in the beginning of the Test phase within the first 30 s. In this interval, the Sleep group displayed exploration preference of the novel juvenile significantly above chance level, and the exploration preference for the novel conspecific was also significantly stronger if compared to those of the Wake group.
Fittingly, in the Sleep rats latency to explore the novel conspecifics was shorter than to explore the familiar one, whereas such difference was not observed in the Wake rats. It might be argued that rather than effects of sleep, the observed differences in exploration preference between the Sleep and Wake animals during the Test phase reflect non-specific effects on memory retrieval, due to the fact that the Wake animals were tested immediately after the min period of enforced wakefulness.
This makes it highly unlikely that the lack of social recognition memory in the Wake rats was a mere consequence of, e. Likewise, stress as a consequence of depriving the rats from sleep, can be ruled out as a factor that substantially affected exploration behavior in the Wake group animals because we chose a rather short period of sleep deprivation min and sleep deprivation was established by the gentle handling procedure.
These conditions are well-known to keep potential stress at a minimum and not to induce substantial increases in blood levels of the stress hormone corticosterone Kopp et al. Moreover, previous experiments of ours Inostroza et al. Also, both adult and juvenile rats were extensively habituated to the experimental setting which included habituation of the juvenile rats to being explored by an adult conspecifics.
Even if there was some vocalization by the juvenile rats, it should have equally affected performance of the Sleep and Wake group animals. Finally, both Sleep and Wake rats displayed comparable learning of the familiar conspecific as indicated by the decrease in exploration time spent with the juvenile rat across the three consecutive sampling sessions of the Learning phase. This assured that Sleep and Wake rats equally well learned to discriminate the familiar juvenile. Thus, the overall pattern of findings justifies to conclude that processes presumably taking place during sleep—rather than at learning or at retrieval—enhanced formation of social recognition memory in the Sleep rats.
Nevertheless, this conclusion needs to be further scrutinized, e. Our paradigm allowed us to test possible interactions between social recognition and spatial memory formation. During the three consecutive sampling sessions the adult rat was exposed to the juvenile rat presented at three different locations in the maze, and the decrease in exploration time across sampling sessions suggested that in both the Sleep and Wake group the rats were able to recognize the juvenile regardless of the location where it was located.
Nevertheless, our results suggest that the formation of social recognition memory during sleep is modulated by spatial information, and depends on where the familiar juvenile was located on the last sampling session before sleep. After sleep, the adult rat showed a significant preference to explore the novel juvenile rat only when this novel juvenile was placed at a location different from that of the familiar juvenile during the last sampling session.
Moreover, these Sleep-Different rats were not only the only group that displayed significantly shorter latencies to explore the novel than the familiar conspecifics, but their latency to explore the novel conspecific was also significantly shorter than that in the respective Wake-Different control group.
Overall, these effects of sleep revealed exclusively in the Sleep-Different group support the view that consolidation processes during sleep do not enhance the social representation of the conspecific per se , but that these processes act primarily on episodic-like representations Kart-Teke et al. Interestingly, the Sleep-Same rats which encountered the novel juvenile at the same place as that of the familiar rat in the last sampling session, also formed significant recognition memory for the juvenile conspecific.
However, this memory expressed only after a substantial delay in the last 3 min of the Test phase. This late onset of preferential exploration of the novel conspecific is difficult to explain, though it corroborates the view that social and spatial memory formation during sleep interact. A previous study provided evidence for competition between two memory domains item vs. In that study, mice failed to show preference for a novel object when the location of a familiar object was changed between learning and testing.
Reversible inactivation of the dorsal hippocampus revealed that object recognition memory per se remained intact in this modified test context, suggesting that such competition affects primarily the expression of memory rather than the memory itself. Accordingly, it is possible that in the present study sleep independently enhanced spatial and social aspects of the sampling sessions experienced before, and that the different dynamics in the expression of exploratory preferences between the Sleep-Different and Sleep-Same group were merely due to the fact that in the latter group, placing the novel juvenile at the same location as that of the familiar juvenile during the last sampling epoch induced competition.
However, this explanation is unlikely for the following reasons: rats of the Sleep-Different group expressed most pronounced exploratory preference in the very beginning, i. By contrast, in the Sleep-Same group a significant exploratory preference for the novel juvenile emerged not until the seventh minute of the Test phase, i. Moreover, analysis of the Sleep-Same rats did not provide any evidence that these rats during the first minute of the Test phase, more strongly engaged in exploring the novel spatial aspects i. However, previous studies have revealed that the concurrent displacement of a familiar object can prevent expression of novel object preference Haettig et al.
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Also, performance during the Learning phase suggested that memory formation as tested in our task does not differently operate depending on whether social or non-social stimuli were employed. Rats of all groups learned to discriminate the familiar juvenile rat across the three sampling sessions as indicated by a most robust decrease in exploration time in the first minute of the min sessions, similar to what is typically seen with non-social objects e. Interestingly, this decrease in exploration time during the Learning phase indicated that the rats learned to recognize the juvenile conspecific independent of its spatial location which changed across sampling sessions which is in stark contrast to the performance of the Sleep-Same animals which during the Test phase showed a distinctly delayed expression of social memory i.
Thus, it appears that spatial context binding does not influence the formation of social recognition memory on the short-term i. It might also be argued that sleep promoted memory for a rule the rats learned across the three sampling sessions of the Learning phase, i. This view assumes that the rat learns to avoid arms of the maze that have been visited most recently. However, this explanation is very unlikely for two reasons: first, rats typically need much more trials than just the three sampling trials of the Learning phase in the present experiments to learn an alternation-like rule where rats requires to avoid the most recent response e.
However, exploration latencies and times in the Sleep-Same rats were very similar for the familiar and novel juveniles. Our study aimed at establishing behavioral evidence that sleep affects the formation of social recognition memory and that this effect might interact with spatial episodic aspects of memory formation. Against this backdrop our study is limited as it does not provide any direct insight into the underlying neurophysiological mechanism of the effect of sleep.
Recent studies have implicated a role of the hippocampal subfield CA2 in social recognition and contextual memory Wintzer et al. Exposure to a conspecific induced remapping of CA2 place fields indicating how CA2 encodes social stimuli by modifying existing spatial representations. The CA2 region was found to be most sensitive in response to subtle changes of familiar spatial context, and remapping of CA2 ensembles for such spatial context also occurred when a familiar or novel conspecific was added to this context Alexander et al.
Together, this evidence suggests that during encoding the hippocampus integrates both social and spatial information into a single episode. Consequently, sleep might benefit social recognition memory by strengthening the integrated neuronal representation of the episode thereby enhancing social information as it is embedded in the spatial context most recently experienced.
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Our results support this view by demonstrating that after sleep the rats rapidly discriminated the familiar and novel conspecifics only in conditions most similar to the recently experienced episode last sampling session , whereas displacing the familiar rat to a novel place attenuated social recognition. In this way the present findings might also be relevant for the understanding of social recognition in healthy humans as well as in patients with social-deficit disorders like autism-spectrum disorders that go along with specific alteration of sleep e.
AS collected the data. AS and EK analyzed the data. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Aggleton, J. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory.
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Rapid encoding of new memories by individual neurons in the human brain. Neuron 87, — Kart-Teke, E. Wistar rats show episodic-like memory for unique experiences. Bound by Recognition. By Patchen Markell. Princeton, N. J: Princeton University Press. Volume 27 , Issue 2. The full text of this article hosted at iucr. If you do not receive an email within 10 minutes, your email address may not be registered, and you may need to create a new Wiley Online Library account.
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