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Sleep-dependent modulation of brain activity. Contrasts are displayed at P 0.001 (uncorrected) superimposed on the average T1-weighted MRI scan. Color bars code the value of the t statistic associated with each voxel. (a) Higher activity elicited by place finding for the RS compared with the TSD group at delayed retrieval bilaterally in the caudate nucleus (sagittal, coronal, and axial sections). Blue crosshair, right caudate nucleus (14, 8, 18 mm; Z 3.73). (b) Between-group regression analyses of the average session performance on cerebral activity at delayed retrieval (sagittal and coronal sections). Blue crosshair, right caudate nucleus (8, 22, 4 mm; Z 3.45). The scatter plot shows that brain response at this coordinate was correlated positively with performance in the RS group (blue; r 0.41) but negatively in the TSD group (red; r 0.80). (c) Psychophysiological interaction analysis using the right caudate nucleus (14, 8, 18 mm; green crosshair) as seed area. The coupling of activity between the caudate nucleus and the left hippocampus (coronal section) was negative in the RS group (blue) but positive in the TSD group (red). Blue crosshair, left hippocampus (22, 12, 22 mm; Z 3.15). Blue and red plots show the size of effect for each group. Error bars are standard deviations.
Source publication
Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later,...
Contexts in source publication
Context 1
... Sleep-Dependent Reorganization of Brain Activity. At delayed retrieval, brain activity during place finding was higher in RS than TSD participants in the right (14,8,18; Z 3.73) and left (16,4,20; Z 3.24) caudate nucleus (p svc(10 mm) 0.05; Fig. 3a) and in several neocortical areas (Table 3). The opposite contrast (i.e., testing for higher brain response in TSD than RS subjects) did not yield any significant results. Posterior proba- bility maps (36) indicated a very low probability of hippocampal activation in between-groups differences at locations in which variations in ...
Context 2
... more (or less) in RS than TSD participants. A significant group by performance interaction was observed in the right caudate nucleus (8, 22, 4; Z 3.45; p svc(10 mm) 0.05), in which blood-oxygen-level-dependent re- sponse was positively coupled with retrieval performance in RS (r 0.41) but negatively coupled in TSD (r 0.80) participants (Fig. 3b). These results indicate that higher involvement of the caudate nucleus during place finding is associated with higher navigation accuracy in the RS group but lower accuracy in the TSD group. Because correlations were computed within each group separately, these correlations are independent from the fact that average activity in the ...
Context 3
... establish distinctive functional connections with other brain regions at delayed retrieval in a posttraining sleep-dependent manner. In RS subjects, coupling between the right caudate nucleus (coordinates, 14, 8, 18 mm) and the left hippocampus (22,12,22) activity was negative, whereas it was positive in the TSD group (Z 3.15, p svc(10 mm) 0.05; Fig. 3c). Similar interaction effects were found in a set of navigation-related neocortical areas (Fig. 4, which is published as supporting information on the PNAS web site). These findings indicate that functional connectivity between the caudate nucleus and the hippocampus was modulated at delayed retrieval by the sleep status on the first ...
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... Sleep can further enhance spatial memories (Ferrara et al., 2008;Samanta et al., 2021;Simon et al., 2022) and have positive effects on strategy flexibility and memory integration (Noack et al., 2021) via memory reactivations (Rasch & Born, 2013). After sleep, humans showed increased navigation-related striatal activity, suggesting a shift from hippocampusdependent to striatum-dependent navigation over time (Orban et al., 2006). In rodents, sleep deprivation can lead to a preference for response over place navigation (Hagewoud et al., 2010). ...
... Sleep quality has previously been associated with spatial navigation performance, where both subjective and objective measures of sleep quality have been linearly associated with poorer virtual spatial navigation performance [7][8][9] , including sleep duration 7 , fragmented sleep 7,8 and insomnia-like symptoms 8 . Experimental sleep deprivation studies have also shown that sleep deprivation results in poorer spatial navigation performance [10][11][12][13] , although other studies report no significant changes in spatial navigation performance following sleep deprivation 14,15 . A recent study from our team also reported a quadratic (U-shaped) association between selfreported sleep duration and virtual spatial navigation performance on SHQ, where mid-range sleep duration was associated with optimal performance 16 . ...
Sleep has been shown to impact navigation ability. However, it remains unclear how different sleep-related variables may be independently associated with spatial navigation performance, and as to whether gender may play a role in these associations. We used a mobile video game app, Sea Hero Quest (SHQ), to measure wayfinding ability in US-based participants. Wayfinding performance on SHQ has been shown to correlate with real-world wayfinding. Participants were asked to report their sleep duration, quality, daytime sleepiness and nap frequency and duration on a typical night (n = 766, 335 men, 431 women, mean age = 26.5 years, range = 18–59 years). A multiple linear regression was used to identify which self-reported sleep variables were independently associated with wayfinding performance. Shorter self-reported sleep durations were significantly associated with worse wayfinding performance in men only. Other self-reported sleep variables showed non-significant trends of association with wayfinding performance. When removing non-typical sleepers (< 6 or > 9 h of sleep on a typical night), the significant association between sleep duration and spatial navigation performance in men was no longer present. These findings from U.S.-based participants suggest that a longer self-reported sleep duration may be an important contributor to successful navigation ability in men.
... There is evidence indicating that sleep is needed to stabilize the hippocampal disengagement effected by repeated encoding and retrieval (Himmer et al., 2019), but it is currently unknown whether sleep also continues to shape neocortical representations. Interestingly, sleep can subserve memory consolidation not only by modulating the contribution of different nodes within a domain-specific mnemonic system (like hippocampus and neocortex within the declarative memory system), but also by the way how entire memory systems interact (Albouy et al., 2013;Cousins et al., 2016;Durrant et al., 2013;Orban et al., 2006). For example, in motor sequence learning, a night of sleep can change the co-activation of the involved declarative and procedural memory systems from a competitive to a cooperative mode (Albouy et al., 2013). ...
... Here, changes in functional connectivity between these systems have been observed across consolidation windows of 24 h and there are indications that these changes might depend on sleep (Albouy et al., 2008;Durrant et al., 2013). Furthermore, in spatial navigation tasks that can be solved with either hippocampus-or striatum-dependent strategies (Doeller et al., 2008), sleep has been shown to affect functional connectivity as well as behavioral strategy usage (Noack et al., 2021;Orban et al., 2006). The nature of hippocampus-striatum interactions seems to depend strongly on the specific task at hand (Freedberg et al., 2020), with some studies reporting decreased functional connectivity after sleep (Durrant et al., 2013;Orban et al., 2006), while others emphasize an integrative function (Albouy et al., 2013;Noack et al., 2021). ...
... Furthermore, in spatial navigation tasks that can be solved with either hippocampus-or striatum-dependent strategies (Doeller et al., 2008), sleep has been shown to affect functional connectivity as well as behavioral strategy usage (Noack et al., 2021;Orban et al., 2006). The nature of hippocampus-striatum interactions seems to depend strongly on the specific task at hand (Freedberg et al., 2020), with some studies reporting decreased functional connectivity after sleep (Durrant et al., 2013;Orban et al., 2006), while others emphasize an integrative function (Albouy et al., 2013;Noack et al., 2021). ...
Sleep benefits memory performance by fostering systems consolidation, a process that embeds memories into neocortical networks and renders them independent of the hippocampus. Recent evidence shows that memory rehearsal during wakefulness likewise initiates systems consolidation and rapidly engenders neocortical engrams. Here, we investigate the effect of sleep-dependent consolidation for memories that have undergone rapid systems consolidation during wakefulness. After sleep compared to wakefulness, we find better memory retention and higher functional brain activity during memory retrieval in the medial parietal cortex, which hosts memory representations after rehearsal, and in the striatum and thalamus. Increased striatal and thalamic contributions were correlated with higher retrieval performance. Furthermore, all three regions decreased their functional connectivity to the hippocampus specifically after sleep. These findings show that besides continuing of systems consolidation initiated during wakefulness, sleep also acts to integrate different memory systems. Thus, rehearsal-induced and sleep-dependent consolidation seem to be complementary in nature.
... However, such an explanation would not be consistent with research accumulated over the last 15 years which has demonstrated that the consolidation of memories formed during motor tasks share common features and rely on similar neural substrates and networks as the consolidation of memories formed during declarative tasks. Specifically, neuroimaging studies have illustrated the involvement of the hippocampal formation in motor sequence learning [43][44][45][46][47][48] and the involvement of the striatum in certain hippocampal-dependent tasks [49][50][51]. The declarative and procedural systems were additionally demonstrated to interact directly, with learning of declarative task interfering with learning of procedural tasks and vice versa [52][53][54]. ...
Study objectives
Novel information is rapidly learned when it is compatible with previous knowledge. This “schema” effect, initially described for declarative memories, was recently extended to the motor memory domain. Importantly, this beneficial effect was only observed 24 hours–but not immediately–following motor schema acquisition. Given the established role of sleep in memory consolidation, we hypothesized that sleep following the initial learning of a schema is necessary for the subsequent rapid integration of novel motor information.
Methods
Two experiments were conducted to investigate the effect of diurnal and nocturnal sleep on schema-mediated motor sequence memory consolidation. In Experiment 1, participants first learned an 8-element motor sequence through repeated practice (Session 1). They were then afforded a 90-minute nap opportunity (N = 25) or remained awake (N = 25) before learning a second motor sequence (Session 2) which was highly compatible with that learned prior to the sleep/wake interval. Experiment 2 was similar; however, Sessions 1 and 2 were separated by a 12-hour interval that included nocturnal sleep (N = 28) or only wakefulness (N = 29).
Results
For both experiments, we found no group differences in motor sequence performance (reaction time and accuracy) following the sleep/wake interval. Furthermore, in Experiment 1, we found no correlation between sleep features (non-REM sleep duration, spindle and slow wave activity) and post-sleep behavioral performance.
Conclusions
The results of this research suggest that integration of novel motor information into a cognitive-motor schema does not specifically benefit from post-learning sleep.
... However, how approaching or reactive children are, might be relevant for performance in the laboratory or learning in the short-term. Performance is not always correlated with learning as successful learning can still occur despite poor performance (Orban et al., 2006;Rieser-Danner, 2003;Soderstrom & Bjork, 2015). This might particularly be the case when it comes to temperament. ...
When hearing a novel word, children typically rule out familiar objects and assume a speaker is referring to a novel object. This strategy is known as fast mapping, and young children use this with a high degree of accuracy. However, not all children engage in fast mapping to the same extent and temperament can play a role. Shyness is associated with poorer fast mapping and less attention to target objects, which is associated with poorer retention (Hilton et al., 2019; Hilton & Westermann, 2017). We further investigated the relationship between temperament and fast mapping by presenting 2.5-year-old children with 8 familiar target fast mapping trials and 4 novel target trials presented twice. We considered two temperamental dimensions: approachability due to its similarity to shyness; and reactivity, which could predict children’s capacity to engage during fast mapping. We found an association between approachability and fast mapping accuracy the second time children fast-mapped novel targets, and approachability was associated with greater retention accuracy. Reactivity predicted proportions of target looking during fast mapping with less reactive temperament scores associated with greater focus on targets. This provides support for a relationship between two dimensions of temperament and fast mapping and retention. Approachability may be associated with a further opportunity to fast map and memory for novel words, and/or how willing children are to guess the targets. Reactivity may be associated with the capacity to focus during word learning situations. Different aspects of temperament could have implications for children’s capacity to disambiguate and learn words.
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... This neural activity correlated with next day behavioral performance improvement. Subsequent studies tested for a specialized role of sleep in spatial memory consolidation by administering Peigneux's virtual navigation task and having participants either sleep or undergo sleep deprivation for the night after learning (30,39). Subsequent testing found no behavioral performance differences between the two conditions; however, participants who slept showed functional reorganization of the spatial memory with increased striatal activity after sleep that correlated with behavioral performance (30,39). ...
... Subsequent studies tested for a specialized role of sleep in spatial memory consolidation by administering Peigneux's virtual navigation task and having participants either sleep or undergo sleep deprivation for the night after learning (30,39). Subsequent testing found no behavioral performance differences between the two conditions; however, participants who slept showed functional reorganization of the spatial memory with increased striatal activity after sleep that correlated with behavioral performance (30,39). Javadi et al. used a similar place-finding virtual navigation task but attempted to strengthen the sleep-dependent aspect by training participants to associate locations with specific value-laden objects (40). ...
Sleep facilitates hippocampal-dependent memories, supporting the acquisition and maintenance of internal representation of spatial relations within an environment. In humans, however, findings have been mixed regarding sleep's contribution to spatial memory and navigation, which may be due to task designs or outcome measurements. We developed the Minecraft Memory and Navigation (MMN) task for the purpose of disentangling how spatial memory accuracy and navigation change over time, and to study sleep's independent contributions to each. In the MMN task, participants learned the locations of objects through free exploration of an open field computerized environment. At test, they were teleported to random positions around the environment and required to navigate to the remembered location of each object. In study 1, we developed and validated four unique MMN environments with the goal of equating baseline learning and immediate test performance. A total of 86 participants were administered the training phases and immediate test. Participants' baseline performance was equivalent across all four environments, supporting the use of the MMN task. In study 2, 29 participants were trained, tested immediately, and again 12 h later after a period of sleep or wake. We found that the metric accuracy of object locations, i.e., spatial memory, was maintained over a night of sleep, while after wake, metric accuracy declined. In contrast, spatial navigation improved over both sleep and wake delays. Our findings support the role of sleep in retaining the precise spatial relationships within a cognitive map; however, they do not support a specific role of sleep in navigation.
... Further, a study that trained participants to find routes through a small network of streets in a virtual reality environment showed that increased hippocampal activity during sleep was related to improved performance after sleep 37 . The same group later demonstrated that sleep can restructure navigational behaviour to become less reliant on a spatial hippocampus dependent strategy and engage an additional striatal stimulus response based strategy 38 . Together these studies suggest that the day after learning a street network the hippocampus is able to track the connectivity in a network during navigation and that navigational memories are reactivated and transformed during sleep. ...
Much of our long-term knowledge is organised in complex networks. Sleep is thought to be critical for abstracting knowledge and enhancing important item memory for long-term retention. Thus, sleep should aid the development of memory for networks and the abstraction of their structure for efficient storage. However, this remains unknown because past sleep studies have focused on discrete items. Here we explored the impact of sleep (night-sleep/day-wake within-subject paradigm with 25 male participants) on memory for graph-networks where some items were important due to dense local connections (degree centrality) or, independently, important due to greater global connections (closeness/betweenness centrality). A network of 27 planets (nodes) sparsely interconnected by 36 teleporters (edges) was learned via discrete associations without explicit indication of any network structure. Despite equivalent exposure to all connections in the network, we found that memory for the links between items with high local connectivity or high global connectivity were better retained after sleep. These results highlight that sleep has the capacity for strengthening both global and local structure from the world and abstracting over multiple experiences to efficiently form internal networks of knowledge.
... However, such an explanation would not be consistent with research accumulated over the last 15 years which has demonstrated that the consolidation processes of declarative and motor memories share common features and rely on similar neural substrates and networks. Specifically, neuroimaging studies have illustrated the involvement of the hippocampal formation in motor sequence learning [45][46][47][48][49][50] and the involvement of the striatum in certain hippocampal-dependent tasks [51][52][53] . The declarative and procedural systems were additionally demonstrated to interact directly, with learning of declarative task interfering with learning of procedural tasks and vice versa [54][55][56] . ...
Study Objectives
Novel information is rapidly learned when it is compatible with previous knowledge. This “schema” effect, initially described for declarative memories, was recently extended to the motor memory domain. Importantly, this beneficial effect was only observed 24 hours – but not immediately – following motor schema acquisition. Given the established role of sleep in memory consolidation, we hypothesized that sleep following the initial learning of a schema is necessary for the subsequent rapid integration of novel motor information.
Methods
Two experiments were conducted to investigate the effect of diurnal and nocturnal sleep on schema-mediated motor sequence memory consolidation. In Experiment 1, participants first learned an 8-element motor sequence through repeated practice (Session 1). They were then afforded a 90-minute nap opportunity (N=25) or remained awake (N=25) before learning a second motor sequence (Session 2) which was highly compatible with that learned prior to the sleep/wake interval. Experiment 2 was similar; however, Sessions 1 and 2 were separated by a 12-hour interval that included nocturnal sleep (N=28) or only wakefulness (N=29).
Results
For both experiments, we found no group differences in motor sequence performance (reaction time and accuracy) following the sleep/wake interval. Furthermore, in Experiment 1, we found no correlation between sleep features (non-REM sleep duration, spindle and slow wave activity) and post-sleep behavioral performance.
Conclusions
The results of this research suggest that integration of novel motor information into a cognitive-motor schema does not specifically benefit from post-learning sleep.
... For example, a positron emission tomography (PET) study by Peigneux et al. found that the degree of hippocampal blood flow during post-learning SWS predicts improvement in a spatial task assessed the following day (Peigneux et al., 2004). Furthermore, a functional magnetic resonance imaging (fMRI) study by Orban et al. demonstrated that post-learning sleep promotes the integration of recently acquired spatial information into hippocampus-related networks (Orban et al., 2006). Another fMRI study by Rauchs et al. examined the effects of post-learning sleep vs. post-learning sleep deprivation on the neural substrates of spatial memory, and found that in subjects who slept after learning, spatial memory was associated with increased posterior cortical activity, while in subjects who underwent sleep deprivation after learning, spatial memory was associated with increased parahippocampal and medial temporal activity (Rauchs et al., 2008). ...
... Participants can perform poorly despite substantial learning, and participants can demonstrate strong performance despite poor learning. Orban, et al. [77] found memory-related changes in brain activity using fMRI despite no clear changes in performance. What does this mean for the fast mapping studies investigated here? ...
Children can easily link a novel word to a novel, unnamed object—something referred to as fast mapping. Despite the ease and speed with which children do this, their memories for novel fast-mapped words can be poor unless they receive memory supports such as further exposure to the words or sleep. Axelsson, Swinton, Winiger, and Horst (2018) found that 2.5-year-old children who napped after fast mapping had better retention of novel words than children who did not nap. Retention declined for those who did not nap. The children received no memory supports and determined the word–object mappings independently. Previous studies report enhanced memories after sleeping in children and adults, but the napping children’s retention in the Axelsson et al. study remained steady across time. We report a follow-up investigation where memory supports are provided after fast mapping to test whether memories would be enhanced following napping. Children’s retention of novel words improved and remained greater than chance; however, there was no nap effect with no significant difference between the children who napped and those who did not. These findings suggest that when memory supports are provided, retention improves, and the word–object mappings remain stable over time. When memory traces are weak and labile, such as after fast mapping, without further memory supports, sleeping soon after helps stabilise and prevent decay of word–object mappings.
