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Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences

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Abstract

Long-term storage of episodic memories is hypothesized to result from the off-line transfer of information from the hippocampus to neocortex, allowing a hippocampal-independent cortical representation to emerge. However, off-line hippocampal-cortical interactions have not been demonstrated to be linked with long-term memory. Here, using functional magnetic resonance imaging, we examined if hippocampal-cortical BOLD correlations during rest following an associative encoding task are related to later associative memory performance. Our data show enhanced functional connectivity between the hippocampus and a portion of the lateral occipital complex (LO) during rest following a task with high subsequent memory compared to pretask baseline resting connectivity. This effect is not seen during rest following a task with poor subsequent memory. Furthermore, the magnitude of hippocampal-LO correlations during posttask rest predicts individual differences in later associative memory. These results demonstrate the importance of postexperience resting brain correlations for memory for recent experiences.

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... Indeed, accumulating evidence in humans has shown that functional connectivity between the hippocampus and the cortex increases after novel learning and predicts memory retrieval success (Tambini et al., 2010;Tompary et al., 2015;de Voogd et al., 2016;Schlichting & Preston, 2016;Murty et al., 2017;Tambini & Davachi, 2019). A critical missing piece of the puzzle, however, is that we lack a comprehensive understanding of which factors modulate offline replay dynamics between the hippocampus and the cortex. ...
... Post-encoding resting state activity has been suggested to support the consolidation of memories which has, in turn, been associated with their behavioral accessibility (Tambini et al., 2010;Deuker et al., 2013;Staresina et al., 2013;Tambini & Davachi, 2013, 2019Schlichting & Preston, 2014;Tompary et al., 2015;Gruber et al., 2016;Murty et al., 2017;Poskanzer et al., 2021). Here, we asked if post-encoding neural replay was related to memory behavior for weakly CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
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No sooner is an experience over than its neural memory representation begins to be strengthened and transformed through the process of memory replay. Using fMRI, we examined how memory strength manipulated through repetition during encoding modulates post-encoding replay in humans. Results revealed that repetition did not increase replay frequency in the hippocampus. However, replay in cortical regions and hippocampal-cortical coordinated replay were significantly enhanced for repeated events, suggesting that repetition accelerates the consolidation process. Interestingly, we found that replay frequency in both hippocampus and cortex modulated behavioral success on an immediate associative recognition test for the weakly encoded information, indicating a significant role for post-encoding replay in rescuing oncepresented events. Together, our findings highlight the relationships of replay to stabilizing weak memories and accelerating cortical consolidation for strong memories.
... Spontaneous cortical activity measured in a task free (resting) state is correlated between brain regions that are jointly recruited in different tasks and cognitive states [1][2][3][4][5][6] . Furthermore, the correlation between cortical regions at rest can be modified by learning, specifically in cortical regions recruited during novel motor, tactile, visual, or memory tasks [7][8][9][10][11][12][13] . These findings indicate that ongoing spontaneous activity in the resting state represent, at least in part, the global structure of behaviorally relevant brain processing. ...
... Participants (N = 15, 7 females, mean age 26.5, all right-handed) performed a blockdesign hand-movement task in which they were instructed by a visual word cue presented on a mirror-set inside the magnet, to move their right hand repeatedly for 10 s in one of four movements followed by a variable rest period (20-24 s), see Fig. 1. The sample size for this study was estimated based on previous studies comparing patterns of spontaneous neural activity to patterns evoked by stimuli 7,8,16 . Moreover, this sample size is largely overlapping with our previous study investigating the spontaneous representational role in the visual cortex 17 . ...
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Spontaneous brain activity, measured with resting state fMRI (R-fMRI), is correlated among regions that are co-activated by behavioral tasks. It is unclear, however, whether spatial patterns of spontaneous activity within a cortical region correspond to spatial patterns of activity evoked by specific stimuli, actions, or mental states. The current study investigated the hypothesis that spontaneous activity in motor cortex represents motor patterns commonly occurring in daily life. To test this hypothesis 15 healthy participants were scanned while performing four different hand movements. Three movements (Grip, Extend, Pinch) were ecological involving grip and grasp hand movements; one control movement involving the rotation of the wrist was not ecological and infrequent (Shake). They were also scanned at rest before and after the execution of the motor tasks (resting-state scans). Using the task data, we identified movement-specific patterns in the primary motor cortex. These task-defined patterns were compared to resting-state patterns in the same motor region. We also performed a control analysis within the primary visual cortex. We found that spontaneous activity patterns in the primary motor cortex were more like task patterns for ecological than control movements. In contrast, there was no difference between ecological and control hand movements in the primary visual area. These findings provide evidence that spontaneous activity in human motor cortex forms fine-scale, patterned representations associated with behaviors that frequently occur in daily life.
... The magnitude of the reactivation seems thereby related to improved memory. Tambini et al. (2010) found enhanced functional connectivity between task-relevant brain areas (hippocampus and a portion of the lateral occipital complex) during rest following a task with high subsequent memory. Furthermore, they found that the magnitude of the correlation between the connectivity of the learning relevant brain areas during rest predicted individual differences in a later memory test (see also Buch et al., 2021). ...
... Our results from Experiment 2 support the view that less concrete words benefit from a state during which attention to external sensory input is reduced (Craig et al., 2014;Dewar et al., 2012;Mednick et al., 2011;Robertson, 2012;Wamsley, 2019;Wixted, 2005). Furthermore, consolidation has been associated with the reactivation of recent experiences (Dudai et al., 2015;Tambini & Davachi, 2019;Tambini et al., 2010). Wakeful resting might just provide conditions of minimal interference, during which previously encoded words can be reactivated more often than is possible during periods filled with listening to music. ...
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Wakeful resting and listening to music are powerful means to modulate memory. How these activities affect memory when directly compared has not been tested so far. In two experiments, participants encoded and immediately recalled two word lists followed by either 6 min wakefully resting or 6 min listening to music. The results of Experiment 1 show that both post-encoding conditions have a similar effect on memory after 1 day. In Experiment 2, we explored the possibility that less concrete words, i.e. lower in imageability than in Experiment 1, are differently affected by the two post-encoding conditions. The results of Experiment 2 show that, when words are less concrete, more words are retained after 1 day when encoding is followed by wakeful resting rather than listening to music. These findings indicate that the effects of wakeful resting and listening to music on memory consolidation are moderated by the concreteness of the encoded material.
... By using multi-site data from ABIDE, we first obtained all participants' dFC whole-brain maps in which the dFC value is estimated by the metric of the percent of signal change. This metric represents the change of bold signal induced by task stimuli relative to the baseline condition in task-based fMRI studies (Kanwisher et al., 1997;Kanwisher et al., 1998;Tambini et al., 2010), as well as the change of the spontaneous bold signal during the whole time course in resting state fMRI (Jia et al., 2020). Then, for ASD and TCs at each site, we calculated the differences of dFC map to obtain the raw t statistical map without correction. ...
... The thalamus is a relay station for the processing of sensory information except olfactory (Gamble, 1986). In general, sensory information is transmitted from the thalamus to the amygdala, and then the amygdala evaluates the emotional meaning of the sensory information (Liddell et al., 2005;Morris et al., 1999;Tambini et al., 2010). In the previous ASD study, lower connectivity between the thalamus and amygdala was found to be associated with more severe symptoms of social interaction (Guo et al., 2016). ...
Article
Background Autism spectrum disorder (ASD) is associated with altered brain connectivity. Previous studies have focused on the static functional connectivity pattern from amygdala subregions in ASD while ignoring its dynamics. Considering that dynamic functional connectivity (dFC) can provide different perspectives, the present study aims to investigate the dFC pattern of the amygdala subregions in ASD patients. Methods Data of 618 ASD patients and 836 typical controls (TCs) of 30 sites were obtained from the Autism Brain Imaging Data Exchange (ABIDE) database. The sliding window approach was applied to conduct seed-based dFC analysis. The seed regions were bilateral basolateral (BLA) and centromedial-superfical amygdala (CSA). Two-sample t-test was done at each site. Image-based meta-analysis (IBMA) based on the results from all sites was performed. Correlation analysis was conducted between the dFC values and the clinical scores. Results The ASD patients showed lower dFC between the left BLA and the bilateral inferior temporal (ITG)/left superior frontal gyrus and between the right BLA and right ITG/right thalamus/left superior temporal gyrus. The ASD patients showed higher dFC between the left BLA and temporal lobe/right supramarginal gyrus, between the right BLA and left calcarine gyrus, between the left CSA and left calcarine gyrus, and between the right CSA and middle temporal gyrus. Correlation analysis revealed that the symptom severity was positively correlated with the dFC between the bilateral BLA and ITG in ASD. Conclusions Abnormal dFC of the specific amygdala subregions may provide new insights into the pathological mechanisms of ASD.
... Previous studies characterized a set of networks in which brain regions co-activate during resting state (Beckmann et al., 2005;Damoiseaux et al., 2006;De Luca et al., 2006;Smith et al., 2009;Biswal et al., 2010;van den Heuvel and Hulshoff Pol, 2010;Yeo et al., 2011;Lv et al., 2018). Resting state functional connectivity may be related to sustained information processing (Gusnard and Raichle, 2001) as well as environment monitoring and internal thought processes (Buckner et al., 2008) that can dynamically change based on the experiences preceding the resting state scan (Daselaar et al., 2010;Sami et al., 2014;Cecchetto et al., 2019) as well as predict task performance that follows the resting state scan (Tambini et al., 2010;Sala-Llonch et al., 2012;López Zunini et al., 2013;Reineberg et al., 2015). ...
... The latter is particularly relevant for the study of psychiatric disorders as it might explain such phenomena as depressive rumination, obsessive thoughts, and other aberrant forms of cognition. Given that the majority of previous studies focused on healthy individuals and administered the resting state scan following stimulus encoding and prior to a memory test (Tambini et al., 2010;Tambini and Davachi, 2013;Schlichting and Prestona, 2014;Tompary et al., 2015;Murty et al., 2017), little is known about how the accuracy of memories acquired prior to the resting state scan is related to functional connectivity within and between resting state networks in individuals with DD, compared to HC. ...
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Previous research indicates that individuals with depressive disorders (DD) have aberrant resting state functional connectivity and may experience memory dysfunction. While resting state functional connectivity may be affected by experiences preceding the resting state scan, little is known about this relationship in individuals with DD. Our study examined this question in the context of object memory. 52 individuals with DD and 45 healthy controls (HC) completed clinical interviews, and a memory encoding task followed by a forced-choice recognition test. A 5-min resting state fMRI scan was administered immediately after the forced-choice task. Resting state networks were identified using group Independent Component Analysis across all participants. A network modeling analysis conducted on 22 networks using FSLNets examined the interaction effect of diagnostic status and memory accuracy on the between-network connectivity. We found that this interaction significantly affected the relationship between the network comprised of the medial prefrontal cortex, posterior cingulate cortex, and hippocampal formation and the network comprised of the inferior temporal, parietal, and prefrontal cortices. A stronger positive correlation between these two networks was observed in individuals with DD who showed higher memory accuracy, while a stronger negative correlation (i.e., anticorrelation) was observed in individuals with DD who showed lower memory accuracy prior to resting state. No such effect was observed for HC. The former network cross-correlated with the default mode network (DMN), and the latter cross-correlated with the dorsal attention network (DAN). Considering that the DMN and DAN typically anticorrelate, we hypothesize that our findings indicate aberrant reactivation and consolidation processes that occur after the task is completed. Such aberrant processes may lead to continuous “replay” of previously learned, but currently irrelevant, information and underlie rumination in depression.
... functional connectivity (FC) patterns over minute-long timescales (Logothetis et al., 2012;Tambini & Davachi, 2019). This allows brain mechanisms related to early consolidation to be studied in MRI paradigms using a baseline (or pre-learning) scan, a memory task, followed by a memory task and a postlearning scan (Deuker et al., 2013;Gruber et al., 2016;Kukolja et al., 2016;Murty et al., 2017Murty et al., , 2019Tambini et al., 2010;Tambini & Davachi, 2013). Changes from pre-to post-learning (e.g., increased FC) can be interpreted as related to the ongoing strengthening of memory traces, especially when related to encoding (Tambini & Davachi, 2019). ...
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Human memory is selective and not all experiences are remembered. Both monetary rewards/incentives and curiosity have been found to motivate and facilitate learning by dopaminergic midbrain projections to the hippocampus during encoding. In this study, we examined potential brain mechanisms during early consolidation period that jointly or independently contribute to these facilitating effects. Participants (N = 50) watched 36 videos of magic tricks and rated their “subjective feelings of curiosity” while the availability of extrinsic incentives was manipulated between groups. Functional magnetic resonance imaging (fMRI) data were acquired before, during, and after learning, and memory for magic tricks was assessed one week after. Our analysis focused on the change in resting-state functional connectivity (RSFC) between the dopaminergic midbrain and the anterior hippocampus, a dopaminergic consolidation mechanism previously reported in the context of extrinsically motivated learning. Changes in RSFC were correlated with behavioural measures of learning, i.e., the total number of items encoded and the curiosity-driven memory benefit. We found that brain-behaviour correlations differed depending on the availability of extrinsic incentives. More specifically, the correlation between the total number of items encoded and RSFC change was significantly different in the incentivised compared to the control group. The curiosity-driven memory benefit, however, did not correlate with changes in RSFC in either of the groups. In sum, this suggests that curiosity-motivated learning might be supported by different consolidation mechanisms compared to extrinsically motivated learning and that extrinsic incentives influence consolidation mechanisms supporting learning. Key points A new curiosity-motivated incidental encoding paradigm was used to investigate how dopaminergic consolidation mechanisms support learning and whether this is further influenced by the availability of monetary incentives. Changes in resting-state functional connectivity between the dopaminergic midbrain and the anterior hippocampus, a dopaminergic consolidation mechanism, predicted learning outcomes significantly differently if monetary incentives were available. These results might suggest that learning motivated by curiosity might rely on different neural mechanisms during early consolidation than learning motivated by monetary incentives.
... First, using a grid for associative learning may have contributed to an increased level of interference, due to the relatively low discriminability of grid locations (compared to using close associates of the presented items). Most prior fMRI work on reactivation has focused on pairs of visual items to test associative memory (e.g., Tambini et al., 2010). Notably, the Diekelmann et al (2011) study discussed above also utilized grid learning to . ...
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Systems consolidation theories posit that consolidation occurs primarily through a coordinated communication between hippocampus and neocortex (McClelland and O'Reilly 1995; Kumaran et al., 2016; Moscovitch and Gilboa, 2022). Recent sleep studies in rodents have shown that hippocampus and visual cortex replay the same information at temporal proximity ("co-replay") (Ji & Wilson, 2007; Lansink et al., 2009; Wierzynski et al., 2009; Peyrache et al., 2009). We developed a novel TR-based co-reactivation (TRCR) analysis method to study hippocampal-cortical co-replays in humans using functional MRI. Thirty-six young adults completed an image (face or scene)-location paired associate encoding task in the scanner, which were preceded and followed by resting state scans. We identified post-encoding rest TRs (+/- 1) that showed neural reactivation of each image-location trials in both hippocampus (HPC) and category-selective cortex (fusiform face area, FFA). This allowed us to characterize temporally proximal coordinated reactivations ("co-reactivations") between HPC and FFA. Moreover, we found that increased HPC-FFA co-reactivations were associated with incorrectly recognized trials after a 1-week delay (p = 0.004). Finally, we found that these HPC-FFA co-reactivations were also associated with trials that were initially correctly recognized immediately after encoding but were later forgotten in 1-day (p = 0.043) and 1-week delay period (p = 0.031). We discuss these results from a trace transformation perspective (Winocur and Moscovitch, 2011; Sekeres et al., 2018) and speculate that HPC-FFA co-reactivations may be integrating related events, at the expense of disrupting event-specific details, hence leading to forgetting.
... Here, the resting state was acquired after a visual task of an extended duration. In the literature on resting state networks, it has been extensively reported that the performance of a task (such as a learning task or memory load) affects brain dynamics during subsequent resting state (e.g., Gordon et al., 2012;Lewis et al., 2009;Pyka et al., 2009;Tambini et al., 2010;Wang et al., 2012). ...
Thesis
The brain’s ongoing activity plays an important role for perception and cognition. In particular, alpha oscillations index arousal and have been linked to fluctuations in perception. Pioneering work has shown that in occipito-parietal brain regions during resting state, alpha oscillations are modulated by the slow rhythm (~0.05 Hz) generated by the stomach, measured non-invasively using the Electrogastrogram. This led us to ask whether the gastric rhythm is coupled to brain alpha oscillations during perceptual tasks and might thereby induce fluctuations in perception. To test this hypothesis, a first aim was to improve and standardize methods to record and analyze the gastric rhythm in healthy participants. We therefore designed and tested a protocol for the recording, preprocessing and analysis of the Electrogastrogram, to extract a regular gastric rhythm. Our second methodological aim was to determine which statistical methodology was sensitive to different profiles of coupling between gastric phase and behavior. I systematically compared the performance of different circular statistical tests and strategies, with respect to experimental parameters and properties of the underlying phase effect. In the third part of my PhD, we then experimentally tested the hypothesis that the gastric rhythm has an influence on fluctuations in visual perception. We found no evidence that gastric phase modulated the probability of target detection. Cortical alpha oscillations were significantly coupled to the gastric rhythm in a large cluster spanning parieto-occipital to mid/frontal sensors. However, individual brain-alpha coupling strength appeared to have no behavioral correlate, since it did not covary with individual hit rate or mean reaction time. In sum, this study for the first time identified gastric-alpha coupling while participants are engaged in a task, but could not identify the behavioral correlate of such coupling, leaving open the question of the functional role of gastric-alpha coupling.
... When we engage in certain behaviors, evoked neural activity causes perturbations to intrinsic connectivity by coupling different neural components, perturbations that persist across multiple timescales (Han et al., 2008;Harmelech et al., 2013). Thus, an individual's intrinsic network configuration at one time point reflects a history of past behavior and environmental inputs (Tambini et al., 2010;Sadaghiani and Kleinschmidt, 2013). From this perspective, developmental changes in brain networks can be understood as emerging from a child's experience that involves active sampling of the external world over the course of development (Berkes et al., 2011;Byrge et al., 2014). ...
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Introduction We have demonstrated that intensive cognitive training can produce sustained improvements in cognitive performance in adolescents. Few studies, however, have investigated the neural basis of these training effects, leaving the underlying mechanism of cognitive plasticity during this period unexplained. Methods In this study, we trained 51 typically developing adolescents on cognitive control tasks and examined how their intrinsic brain networks changed by applying graph theoretical analysis. We hypothesized that the training would accelerate the process of network integration, which is a key feature of network development throughout adolescence. Results We found that the cognitive control training enhanced the integration of functional networks, particularly the cross-network integration of the cingulo-opercular network. Moreover, the analysis of additional data from older adolescents revealed that the cingulo-opercular network was more integrated with other networks in older adolescents than in young adolescents. Discussion These findings are consistent with the hypothesis that cognitive control training may speed up network development, such that brain networks exhibit more mature patterns after training.
... Previous work has indicated that spontaneous cortical activity, measured in a task free (resting) state, is correlated between brain regions that are jointly recruited in different task and cognitive states (Golland et al., 2008;Greicius et al., 2003;Nir et al., 2006;Power et al., 2010;Raichle et al., 2001;Xiong et al., 2009). Furthermore, the correlation between cortical regions at rest can be modified by learning, specifically in regions recruited by a novel task pattern (Albert et al., 2009;Harmelech et al., 2013;Lewis et al., 2009;McGregor and Gribble, 2015;Tambini et al., 2010). These findings suggest that ongoing correlated patterns of brain activity represent, at least in part, the global structure of behaviorally relevant brain processing. ...
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Spontaneous neural activity has been shown to preserve the inter-regional structure of cortical activity evoked by a task. It is unclear, however, whether patterns of spontaneous activity within a cortical region comprise representations associated with specific behaviors or mental states. The current study investigated the hypothesis that spontaneous neural activity in human motor cortex represents motor responses that commonly occur in daily life. To test this hypothesis 15 healthy participants were scanned in a 3T fMRI scanner while performing four simple hand movements differing by their daily life relevance, and while not performing any specific task (resting-state scans). Using the task data, we identified cortical patterns in a motor ROI corresponding to the different hand movements. These task-defined patterns were compared to spontaneous cortical activity patterns in the same motor ROI. The results indicated a higher similarity of the spontaneous patterns to the most common hand movement than to the least common hand movement. This finding provides the first evidence that spontaneous activity in human cortex forms fine-scale, patterned representations associated with behaviors that frequently occur in daily life.
... Such reactivations involve temporally condensed, hyper-synchronous events that occur during quiet waking and sleep 1,[11][12][13] . First observed and most commonly studied in the hippocampus, reactivations have also been observed in the amygdala, prefrontal cortex, visual cortex, striatum and elsewhere [15][16][17][18][19][20][21][22][23][24][25][26][27][28][29] . ...
Preprint
Prevailing theories of offline memory consolidation posit that the pattern of neurons activated during a salient sensory experience will be faithfully reactivated, thereby stabilizing the entire pattern ¹⁻³ . However, sensory-evoked patterns are not stable, but instead drift across repeated experiences ⁴⁻⁷ . To investigate potential roles of reactivations in the stabilization and/or drift of sensory representations, we imaged calcium activity of thousands of excitatory neurons in mouse lateral visual cortex. Presentation of a stimulus resulted in transient, stimulus-specific reactivations during the following minute. These reactivations depended on local circuit activity, as they were abolished by local silencing during the preceding stimulus. Contrary to prevailing theories, reactivations systemically differed from previous patterns evoked by the stimulus. Instead, they were more similar to future patterns evoked by the stimulus, thereby predicting representational drift. In particular, neurons that participated more or less in early reactivations than in stimulus response patterns subsequently increased or decreased their future stimulus responses, respectively. The rate and content of these reactivations was sufficient to accurately predict future changes in stimulus responses and, surprisingly, the decreasing similarity of responses to distinct stimuli. Thus, activity patterns during sensory cortical reactivations may guide the drift in sensory responses to improve sensory discrimination ⁸ .
... For example, visual perceptual learning was shown to modulate spontaneous connectivity between the visual and fronto-parietal networks engaged by the task (Lewis et al. 2009). Associative cortical areas and hippocampus increased connectivity following a visual encoding task (both in real life Tambini et al. 2010; and in virtual reality Gauthier et al. 2020). Frontoparietal and cerebellar networks functional connectivity strengthened after exposure to a visuomotor adaptation (Albert et al. 2009). ...
Article
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Our everyday life summons numerous novel sensorimotor experiences, to which our brain needs to adapt in order to function properly. However, tracking plasticity of naturalistic behavior and associated brain modulations is challenging. Here, we tackled this question implementing a prism adaptation-like training in virtual reality (VRPA) in combination with functional neuroimaging. Three groups of healthy participants (N = 45) underwent VRPA (with a shift either to the left/right side, or with no shift), and performed functional magnetic resonance imaging (fMRI) sessions before and after training. To capture modulations in free-flowing, task-free brain activity, the fMRI sessions included resting-state and free-viewing of naturalistic videos. We found significant decreases in spontaneous functional connectivity between attentional and default mode (DMN)/fronto-parietal networks, only for the adaptation groups, more pronouncedly in the hemisphere contralateral to the induced shift. In addition, VRPA was found to bias visual responses to naturalistic videos: Following rightward adaptation, we found upregulation of visual response in an area in the parieto-occipital sulcus (POS) only in the right hemisphere. Notably, the extent of POS upregulation correlated with the size of the VRPA-induced after-effect measured in behavioral tests. This study demonstrates that a brief VRPA exposure can change large-scale cortical connectivity and correspondingly bias visual responses to naturalistic sensory inputs.
... This raises the question of the exact differences between practice and fatigue for participants. One important factor seems to be time or duration (Helton & Russell, 2015;Ross et al., 2014) between the sessions to allow offline processing mechanisms in the brain (Tambini et al., 2010;Wamsley, 2019). Thus, practice interventions usually extend over several weeks (Dux et al., 2009;Hazeltine et al., 2006;Strobach et al., 2014) Additionally, some studies suggested that it is crucial to eliminate any motivation and engagement such as feedback, sense of time, and reward, to establish the state of fatigue (Hopstaken et al., 2015;Katzir et al., 2020;Nakagawa et al., 2013). ...
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The mechanisms underlying increased dual-task costs in the comparison of modality compatible stimulus-response mappings (e.g., visual-manual, auditory-vocal) and modality incompatible mappings (e.g., visual-vocal, auditory-manual) remain elusive. To investigate whether additional control mechanisms are at work in simultaneously processing two modality incompatible mappings, we applied a transfer logic between both types of dual-task mappings in the context of a mental fatigue induction. We expected an increase in dual-task costs for both modality mappings after a fatigue induction with modality compatible tasks. In contrast, we expected an additional, selective increase in modality incompatible dual-task costs after a fatigue induction with modality incompatible tasks. We tested a group of 45young individuals (19-30 years) in an online pre-post design, in which participants were assigned to one of three groups. The two fatigue groups completed a 90-min time-on-task intervention with a dual task comprising either compatible or incompatible modality mappings. The third group paused for 90 min as a passive control group. Pre and post-session contained single and dual tasks in both modality mappings for all participants. In addition to behavioral performance measurements, seven subjective items (effort, focus, subjective fatigue, motivation, frustration, mental and physical capacity) were analyzed. Mean dual-task performance during and after the intervention indicated a practice effect instead of the presumed fatigue effect for all three groups. The modality incompatible intervention group showed a selective performance improvement for the modality incompatible mapping but no transfer to the modality compatible dual task. In contrast, the compatible intervention group showed moderately improved performance in both modality map-pings. Still, participants reported increased subjective fatigue and reduced motivation after the fatigue intervention. This dynamic interplay of training and fatigue effects suggests that high control demands were involved in the prolonged performance of a modality incompatible dual task, which are separable from modality compatible dual-task demands.
... Objective measures can therefore more directly shed light on how sleep benefits memory processes. At the system level, memory consolidation involves an active reinstatement of memory-related brain networks during the subsequent sleep period (Peigneux et al., 2004;Bergmann et al., 2012;Fogel et al., 2017), but also during post-training quiet resting-state (Tambini et al., 2010;Vahdat et al., 2011;Jacobs et al., 2015;Mary et al., 2017). Fang et al. showed that a daytime nap strengthens resting-state FC within the striato-cortico-hippocampal network after motor learning in young adults, whereas this FC is decreased in older adults. ...
... Moreover, numerous studies have demonstrated specific effects of different cognitive and behavioural contexts on resting-state activity. [ Gordon et al., 2014, Tambini et al., 2010 These cognitive contexts could not be entirely controlled from session to session and therefore may have contributed to cross-session variability. Nonetheless, our results from this exploratory study suggest a high level of inter-session correlation and low cross-session variability overall. ...
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Background: When characterizing the brain's resting state functional connectivity (RSFC) networks, demonstrating networks' similarity across sessions and reliability across different scan durations is essential for validating results and possibly minimizing the scanning time needed to obtain stable measures of RSFC. Recent advances in optical functional neuroimaging technologies have resulted in fully wearable devices that may serve as a complimentary tool to functional magnetic resonance imaging (fMRI) and allow for investigations of RSFC networks repeatedly and easily in non-traditional scanning environments. Methods: Resting-state cortical hemodynamic activity was repeatedly measured in a single individual in the home environment during COVID-19 lockdown conditions using the first ever application of a 24-module (72 sources, 96 detectors) wearable high-density diffuse optical tomography (HD-DOT) system. Twelve-minute recordings of resting-state data were acquired over the pre-frontal and occipital regions in fourteen experimental sessions over three weeks. As an initial validation of the data, spatial independent component analysis was used to identify RSFC networks. Reliability and similarity scores were computed using metrics adapted from the fMRI literature. Results: We observed RSFC networks over visual regions (visual peripheral, visual central networks) and higher-order association regions (control, salience and default mode network), consistent with previous fMRI literature. High similarity was observed across testing sessions and across chromophores (oxygenated and deoxygenated haemoglobin, HbO and HbR) for all functional networks, and for each network considered separately. Stable reliability values (described here as a
... Prior research suggests that post-encoding connectivity in memoryrelevant networks reflects early systems consolidation processes, with enhanced delayed long-term retrieval associated with increased connectivity [45][46][47] . The anterior hippocampus has greater structural and functional connectivity to the mPFC than the posterior hippocampus 42,[48][49][50] , and coupling between the anterior hippocampus and mPFC has proven to be related to mnemonic representation and retrieval of remote memories 41,51 . ...
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Memory transformation is increasingly acknowledged in theoretical accounts of systems consolidation, yet how memory quality and neural representation change over time and how schemas influence this process remains unclear. We examined the behavioral quality and neural representation of schema-congruent and incongruent object-scene pairs retrieved across 10-minutes and 72-hours using fMRI. When a congruent schema was available, memory became coarser over time, aided by post-encoding coupling between the anterior hippocampus and medial prefrontal cortex (mPFC). Only schema-congruent representations were integrated in the mPFC over time, and were organized according to schematic context. In the hippocampus, pattern similarity changed across 72-hours such that the posterior hippocampus represented specific details and the anterior hippocampus represented the general context of specific memories, irrespective of congruency. Our findings suggest schemas are used as a scaffold to facilitate neocortical integration of congruent information, and illustrate evolution in hippocampal organization of detailed contextual memory over time.
... The HF plays a significant role in the MTL-subsystem, the resting MTL activity, and the MTL-cortical FC, which were related to individual differences in memory, (Wig et al., 2008) spontaneous episodic thoughts, (Andrews-Hanna et al., 2010a) and the consolidation of recent experiences. (Tambini et al., 2010) Our results revealed that the HF showed significantly different correlation coefficients as compared to other ROIs in DMN between the IACP group and the NACP group, and the FCS between the HF and brain regions in DMN was correlated with the cognitive performance. However, no significant difference in both left and right hippocampal volumes between the IACP and the NACP groups was found. ...
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Adamantinomatous craniopharyngioma (ACPs) are rare embryonic tumors and often involve the hypothalamus. The underlying neural substrate of the hypothalamic involvement (HI)-related cognitive decline in patients with ACP is still unclear. We aimed to combine the multi-modal neuroimaging and histological characteristics of the ACP to explore the potential neural substrate of the HI-related cognitive decline. 45 patients with primary ACPs (invasive, 23; noninvasive, 22) and 52 healthy control subjects (HCs) were admitted to the cross-sectional study. No significant difference in cognitive domains was observed between HCs and patients with noninvasive ACPs (NACP). Patients with invasive ACPs (IACP) showed significantly lower working memory performance (WM, p=0.002) than patients with NACP. The WM decline was correlated with the disruption of the medial temporal lobe (MTL) subsystem in the default mode network (DMN) (r=0.45, p=0.004). The increased radial diffusivity of the fornix, indicating demyelinating process, was correlated with the disruption of the MTL subsystem (r=-0.48, p=0.002). Our study demonstrated that the fornix alterations link DMN disruption to HI-related cognitive decline in patients with ACPs. ACPs that invade the hypothalamus can provide a natural disease model to investigate the potential neural substrate of HI-related cognitive decline.
... SynOT exposure has been found to reduce rest time in the first hour of neonates 20 . Areas of the hippocampus and cortex are more active at times of rest 28 , and the hippocampus, with its clusters of OTRs, is the part of the brain associated with solidifying memories and social behavior and bonding 29,30 . Less rest time is not conducive to consolidating memories and facilitating self-attachment of breasts in newborns 31,32 and it can also affect the start of breastfeeding. ...
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Abstract Synthetic oxytocin is the current domestic first-line agent of induced labor and labor augmentation, and its potential effects on neonatal neurobehavioral development is currently attracting increased attention. To explore the effect of different doses of synthetic oxytocin on neonatal instinctive breastfeeding behavior and breastfeeding by observing neonatal behaviors during skin-to-skin contact with mothers after delivery. Observations and comparisons of neonatal instinctive behaviors were conducted by using Widström's 9 Stages method. According to the total dosage of oxytocin administered during labor, participants were divided into a low dose group (≤ 2.5 U) of 39 pairs, a medium dose group (> 2.5 U) of 38 pairs, a high dose group (> 7.5 U) of 38 pairs and a control group (no synthetic oxytocin use) of 39 pairs. The occurrence time of newborns' instinctive movements and the duration of each behavior stage for the four groups were also analyzed. The number of exclusive breastfeeding sessions within 3 days after birth and the rate of exclusive breastfeeding at 3 months were collected and compared. There were significant differences among the four groups in the occurrence time of raising head or turning head (p = 0.004), eating hands (p = 0.011), moving body (p = 0.001), locating areola (p
... Although many studies have tried to predict rather stable traits, resting-state measures may not display the same level of within-subject stability. Indeed, several studies on healthy participants reported resting-state functional connectivity changes to the hippocampus after an associative memory task (Tambini et al., 2010), to the dorsal attention network, default mode network, and visual networks after a perceptual learning task (Lewis et al., 2009), to motor areas after a finger-tapping task (Sarabi et al., 2018), or to the olfactory piriform cortex after an olfactory task (Cecchetto et al., 2019;Sarabi et al., 2018)). This indicates that the psychological state . ...
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Resting-state functional connectivity has generated great hopes as a potential brain biomarker for improving prevention, diagnosis, and treatment in psychiatry. This neuroimaging protocol can routinely be performed by patients and does not depend on the specificities of a task. Thus, it seems ideal for big data approaches that require aggregating data across multiple studies and sites. However, technical variability, diverging data analysis approaches, and differences in data acquisition protocols might introduce heterogeneity to the aggregated data. Besides these technical aspects, the psychological state of participants might also contribute to heterogeneity. In healthy participants, studies have shown that behavioral tasks can influence resting-state measures, but such effects have not yet been reported in clinical populations. Here, we fill this knowledge gap by comparing resting-state functional connectivity before and after clinically relevant tasks in two clinical conditions, namely substance use disorders and phobias. The tasks consisted of viewing craving-inducing and spider anxiety provoking pictures that are frequently used in cue-reactivity studies and exposure therapy. We found distinct pre- vs. post-task resting-state connectivity differences in each group, as well as decreased thalamo-cortical and increased intra-thalamic connectivity which might be associated with decreased vigilance in both groups. Notably, the pre- vs. post-task thalamus-amygdala connectivity change within a patient cohort seems more pronounced than the difference of that connection between the smoker vs. phobia clinical trait. Our results confirm that resting-state measures can be strongly influenced by changes in psychological states that need to be taken into account when pooling resting-state scans for clinical biomarker detection. This demands that resting-state datasets should include a complete description of the experimental design, especially when a task preceded data collection.
... Individual differences in brain connectivity at rest correlate with differences in behavior (Vaidya and Gordon 2013;Smith et al. 2015). Moreover, learning and behavioral intervention produce measurable changes in FC in relevant cortical circuits and resting correlation is altered by learning and adaptation (Albert et al. 2009;Lewis et al. 2009;Tambini et al. 2010;Sampaio-Baptista et al. 2015;Newbold 2020). Thus, the process of learning that is so fundamental to brain function involves not only modulating processing within a brain area, but also reweighting of functional connections between multiple brain areas. ...
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Understanding the relationships between brain organization and behavior is a central goal of neuroscience. Traditional teaching emphasizes that the human cerebrum includes many distinct areas for which damage or dysfunction would lead to a unique and specific behavioral syndrome. This teaching implies that brain areas correspond to encapsulated modules that are specialized for specific cognitive operations. However, empirically, local damage from stroke more often produces one of a small number of clusters of deficits and disrupts brain-wide connectivity in a small number of predictable ways (relative to the vast complexity of behavior and brain connectivity). Behaviors that involve shared operations show correlated deficits following a stroke, consistent with a low-dimensional behavioral space. Because of the networked organization of the brain, local damage from a stroke can result in widespread functional abnormalities, matching the low dimensionality of behavioral deficit. In alignment with this, neurological disease, psychiatric disease, and altered brain states produce behavioral changes that are highly correlated across a range of behaviors. We discuss how known structural and functional network priors in addition to graph theoretical concepts such as modularity and entropy have provided inroads to understanding this more complex relationship between brain and behavior. This model for brain disease has important implications for normal brain-behavior relationships and the treatment of neurological and psychiatric diseases.
... Moreover, extensive research has established that the networks identified during restingstate may mimic those identifiable with a lot of task paradigms. In other words, activity and connectivity of these networks at rest can be a biomarker of behavioral performance and further function of the same brain regions during task paradigms [51][52][53]. ...
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This study set out to assess restingstate functional connectivity (rs-FN) and graph theorybased local efficiency within the left and right hemispheres of methamphetamine (MA) abusers. Functional brain networks of 19 MA abusers and 21 control participants were analyzed using restingstate fMRI. Graph edges in functional networks of the brain were defined and recurrence plot was used. We found that MA abuse may be accompanied by alterations of rs-FN within the defaultmode network (DMN), executive control network (ECN), and the salience network (SN) in both hemispheres of the brain. We also observed that such effects of MA may be correlated with duration of MA abuse and abstinence in many components of the DMN and SN. The results would seem to suggest that MAinduced alterations of local efficiency may, in part, account for maladaptive decision making, deficits in executive function and control over drug seeking/taking, and relapse.
... Based on resting-state functional magnetic resonance imaging (rsfMRI), functional connectivity (FC) measured as the statistical relationship between regional hemodynamic activities has been found to form large-scale resting-state networks (RSNs) that associate with cognition and its age-related disorders at the system level (Biswal et al., 1995;Craddock et al., 2013;Mill et al., 2017). For instance, FC correlates with and predicts memory performance and can be reshaped by learning, indicating strong behavioral relevance of the RSNs (Albert et al., 2009;Bassett et al., 2011;Kao et al., 2020;Tambini et al., 2010). The disruption of RSNs in association with cognitive impairment and neuropathology provide further evidence for the involvement of these networks in the etiology and progression in diseases (Greicius et al., various forms of spatial memory trace (engram) in these areas suggests that a common network may be involved in the system consolidation of memory [ref] . ...
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Resting-state networks (RSNs) detected by fMRI have been associated with cognitive function, providing insights to the relationship between brain and behavior. However, whether altered RSNs are epiphenomena or essential constructs of behavior remains unclear. Here we investigated whether post-encoding RSN hubs that are commonly engaged after similar tasks or integrate distributed areas into large networks are causally involved in memory consolidation. RSN changes following two types of spatial memory training in mice, allowing us to distinguish post-encoding hubs related to spatial memory, and verify their behavioral impact by hub inhibition. We found that functional connectivity with sensory areas was commonly strengthened in both tasks whereas frontal and striatal areas were influential in network integration. Chemogenetic suppression of each hub after learning resulted in retrograde amnesia. These results demonstrate causal and functional roles of RSN hubs in system consolidation and validate fMRI as a means to track this process.
... Important nodes of these reactivations are thought to incorporate the hippocampal network centered on the medial temporal cortex and retrosplenial cortex (van Buuren et al., 2019), as well as interactions between hubs of the default mode network (Lin et al., 2017) and task-relevant networks (e.g., the executive control network; Sneve et al., 2017). Greater levels of resting-state functional connectivity between areas specific to the stimuli and the hippocampus were shown to predict the future ability to retrieve a memory (Tambini et al., 2010). In addition, functional connectivity immediately after learning as well as the amount of hippocampal reactivation predicted subsequent overnight memory retention, suggesting a complementary relationship between awake resting reactivation and later consolidation during sleep (Schapiro et al., 2018). ...
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After experiences are encoded, post‐encoding reactivations during sleep have been proposed to mediate long‐term memory consolidation. Spindle–slow oscillation coupling during NREM sleep is a candidate mechanism through which a hippocampal‐cortical dialogue may strengthen a newly formed memory engram. Here, we investigated the role of fast spindle‐ and slow spindle–slow oscillation coupling in the consolidation of spatial memory in humans with a virtual watermaze task involving allocentric and egocentric learning strategies. Furthermore, we analyzed how resting‐state functional connectivity evolved across learning, consolidation, and retrieval of this task using a data‐driven approach. Our results show task‐related connectivity changes in the executive control network, the default mode network, and the hippocampal network at post‐task rest. The hippocampal network could further be divided into two subnetworks of which only one showed modulation by sleep. Decreased functional connectivity in this subnetwork was associated with higher spindle–slow oscillation coupling power, which was also related to better memory performance at test. Overall, this study contributes to a more holistic understanding of the functional resting‐state networks and the mechanisms during sleep associated to spatial memory consolidation.
... For example, different kinds of physical inferences (inferring weight vs. predicting dynamics) might map to different parts of the dACC and corresponding frontoparietal cortex. Additionally, a limitation in resting-state connectivity studies can be the effect of previous tasks (Grigg & Grady, 2010;Hasson et al., 2009;Tambini et al., 2010;Wang et al., 2012). As explained in Section 2, one of the resting state scans was collected at the beginning of the scanning session, and another was collected at the end, after a series of intuitive physics tasks. ...
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Recent work has identified brain areas that are engaged when people predict how the physical behavior of the world will unfold – an ability termed intuitive physics. Among the many unanswered questions about the neural mechanisms of intuitive physics is where the key inputs come from: which brain regions connect up with intuitive physics processes to regulate when and how they are engaged in service of our goals? In the present work, we targeted the dorsal anterior cingulate cortex (dACC) for study based on characteristics that make it well‐positioned to regulate intuitive physics processes. The dACC is richly interconnected with frontoparietal regions and is implicated in mapping contexts to actions, a process that would benefit from physical predictions to indicate which action(s) would produce the desired physical outcomes. We collected resting state functional MRI data in seventeen participants and used independent task‐related runs to find the pattern of activity during a physical inference task in each individual participant. We found that the strongest resting state functional connections of the dACC not only aligned well with physical inference‐related activity at the group level, it also mirrored individual differences in the positioning of physics‐related activity across participants. Our results suggest that the dACC might be a key structure for regulating the engagement of intuitive physics processes in the brain.
... Outside of a "representation rich" approach, studies probing the functional relevance of resting-state activity typically link physiological features (e.g., functional connectivity) to behavioural measures of task performance collected before, or after, a resting session. For example, using fMRI, Tambini, et al. 65 reported enhanced functional 30 connectivity between hippocampus and lateral occipital cortex during rest following an associative memory encoding task, which was related to later memory performance. This approach is analogous to linking electrophysiological signatures of reactivation (e.g., SWRs) to memory consolidation in rodents 42 . ...
Article
In human neuroscience, studies of cognition are rarely grounded in non-task-evoked, ‘spontaneous’ neural activity. Indeed, studies of spontaneous activity tend to focus predominantly on intrinsic neural patterns (for example, resting-state networks). Taking a ‘representation-rich’ approach bridges the gap between cognition and resting-state communities: this approach relies on decoding task-related representations from spontaneous neural activity, allowing quantification of the representational content and rich dynamics of such activity. For example, if we know the neural representation of an episodic memory, we can decode its subsequent replay during rest. We argue that such an approach advances cognitive research beyond a focus on immediate task demand and provides insight into the functional relevance of the intrinsic neural pattern (for example, the default mode network). This in turn enables a greater integration between human and animal neuroscience, facilitating experimental testing of theoretical accounts of intrinsic activity, and opening new avenues of research in psychiatry. There is a dichotomy in human neuroscience research between task-based cognition and characterization of intrinsic neural patterns (for example, resting-state networks), In this Review, Liu and colleagues discuss a new paradigm for bridging this gap based on decoding of task-related representations.
... Another outstanding question regarding replay is, despite being associated with subsequent memory (Zhang et al. 2018), it is not clear where in the brain replay makes a demonstrable contribution toward generalization. Replay has been observed throughout the brain, early in the ventral visual stream (Ji and Wilson 2007;Deuker et al. 2013;Wittkuhn and Schuck 2021), in the ventral temporal cortex (Tambini et al. 2010;de Voogd et al. 2016), the medial temporal lobe (Staresina et al. 2013;Schapiro et al. 2018) the amygdala, (Girardeau et al. 2017;Hermans et al. 2017), motor cortex (Eichenlaub et al. 2020), and prefrontal cortex (Peyrache et al. 2009). It is not known if replay in lower-level brain regions actually contributes to the observed memory improvements or whether the key neural changes are made in more advanced areas, and this question cannot be answered using current neuroimaging approaches. ...
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Replay can consolidate memories through offline neural reactivation related to past experiences. Category knowledge is learned across multiple experiences, and its subsequent generalization is promoted by consolidation and replay during rest and sleep. However, aspects of replay are difficult to determine from neuroimaging studies. We provided insights into category knowledge replay by simulating these processes in a neural network which approximated the roles of the human ventral visual stream and hippocampus. Generative replay, akin to imagining new category instances, facilitated generalization to new experiences. Consolidation-related replay may therefore help to prepare us for the future as much as remember the past. Generative replay was more effective in later network layers functionally similar to the lateral occipital cortex than layers corresponding to early visual cortex, drawing a distinction between neural replay and its relevance to consolidation. Category replay was most beneficial for newly acquired knowledge, suggesting replay helps us adapt to changes in our environment. Finally, we present a novel mechanism for the observation that the brain selectively consolidates weaker information, namely a reinforcement learning process in which categories were replayed according to their contribution to network performance. This reinforces the idea of consolidation-related replay as an active rather than passive process.
... However, this could not explain why symptoms that were related to the FC of interest (brooding and general depressive symptoms) decreased but other symptoms (anxiety) did not (but it is possible that successful self-regulation of neural activity simply affects different types of symptoms differently). Finally, the fact that our participants had their resting-state scans taken after the main task on each day of experimentation could mean that their resting state scans did not reflect truly intrinsic activations (see [75][76][77] ). Nonetheless, because our main analyses involved subtracting data from Day 0 away from data from Day 4, and because the task on each of these days was identical, any task-relevant activations should have been subtracted away from the results. ...
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Depressive disorders contribute heavily to global disease burden; This is possibly because patients are often treated homogeneously, despite having heterogeneous symptoms with differing underlying neural mechanisms. A novel treatment that can directly influence the neural circuit relevant to an individual patient’s subset of symptoms might more precisely and thus effectively aid in the alleviation of their specific symptoms. We tested this hypothesis in a proof-of-concept study using fMRI functional connectivity neurofeedback. We targeted connectivity between the left dorsolateral prefrontal cortex/middle frontal gyrus and the left precuneus/posterior cingulate cortex, because this connection has been well-established as relating to a specific subset of depressive symptoms. Specifically, this connectivity has been shown in a data-driven manner to be less anticorrelated in patients with melancholic depression than in healthy controls. Furthermore, a posterior cingulate dominant state—which results in a loss of this anticorrelation—is expected to specifically relate to an increase in rumination symptoms such as brooding. In line with predictions, we found that, with neurofeedback training, the more a participant normalized this connectivity (restored the anticorrelation), the more related (depressive and brooding symptoms), but not unrelated (trait anxiety), symptoms were reduced. Because these results look promising, this paradigm next needs to be examined with a greater sample size and with better controls. Nonetheless, here we provide preliminary evidence for a correlation between the normalization of a neural network and a reduction in related symptoms. Showing their reproducibility, these results were found in two experiments that took place several years apart by different experimenters. Indicative of its potential clinical utility, effects of this treatment remained one-two months later. Clinical trial registration: Both experiments reported here were registered clinical trials (UMIN000015249, jRCTs052180169).
... Resting state FC represents a means of investigating plasticity without confounding goal-directed neuronal action and external muscle outputs. It has also been shown to represent the engagement of the neural networks during motor tasks (Deco et al., 2011) and are predictive of subsequent motor performance (Hampson et al., 2006;Tambini et al., 2010;Wu et al., 2014). Research also indicates that FC measures at rest are biomarkers of cortical function post-stroke (Zhu et al., 2010;Rehme et al., 2011;Dubovik et al., 2012;Wu et al., 2015). ...
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We have developed a passive and lightweight wearable hand exoskeleton (HandSOME II) that improves range of motion and functional task practice in laboratory testing. For this longitudinal study, we recruited 15 individuals with chronic stroke and asked them to use the device at home for 1.5 h per weekday for 8 weeks. Subjects visited the clinic once per week to report progress and troubleshoot problems. Subjects were then given the HandSOME II for the next 3 months, and asked to continue to use it, but without any scheduled contact with the project team. Clinical evaluations and biomechanical testing was performed before and after the 8 week intervention and at the 3 month followup. EEG measures were taken before and after the 8 weeks of training to examine any recovery associated brain reorganization. Ten subjects completed the study. After 8 weeks of training, functional ability (Action Research Arm Test), flexor tone (Modified Ashworth Test), and real world use of the impaired limb (Motor Activity Log) improved significantly ( p < 0.05). Gains in real world use were retained at the 3-month followup ( p = 0.005). At both post-training and followup time points, biomechanical testing found significant gains in finger ROM and hand displacement in a reaching task ( p < 0.05). Baseline functional connectivity correlated with gains in motor function, while changes in EEG functional connectivity paralleled changes in motor recovery. HandSOME II is a low-cost, home-based intervention that elicits brain plasticity and can improve functional motor outcomes in the chronic stroke population.
... For example, visual perceptual learning was shown to modulate spontaneous connectivity between the visual and fronto-parietal networks engaged by the task (Lewis et al., 2009). Associative cortical areas and hippocampus increased connectivity following a visual encoding task (both in real life Tambini et al., 2010; and in virtual reality Gauthier et al., 2020). Frontoparietal and cerebellar networks functional connectivity strengthened after exposure to a visuomotor adaptation (Albert et al., 2009). ...
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Our everyday life summons numerous novel sensorimotor experiences, to which our brain needs to adapt in order to function properly. However, tracking plasticity of naturalistic behaviour and associated brain modulations is challenging. Here we tackled this question implementing a prism adaptation training in virtual reality (VRPA) in combination with functional neuroimaging. Three groups of healthy participants (N=45) underwent VRPA (with a spatial shift either to the left/right side, or with no shift), and performed fMRI sessions before and after training. To capture modulations in free-flowing, task-free brain activity, the fMRI sessions included resting state and free viewing of naturalistic videos. We found significant decreases in spontaneous functional connectivity between large-scale cortical networks – namely attentional and default mode/fronto-parietal networks - only for adaptation groups. Additionally, VRPA was found to bias visual representations of naturalistic videos, as following rightward adaptation, we found upregulation of visual response in an area in the parieto-occipital sulcus (POS) in the right hemisphere. Notably, the extent of POS upregulation correlated with the size of the VRPA induced after-effect measured in behavioural tests. This study demonstrates that a brief VRPA exposure is able to change large-scale cortical connectivity and correspondingly bias the representation of naturalistic sensory inputs. Significance statement In the current work, we tested how a brief sensorimotor experience changes subsequent brain activity and connectivity. Using virtual reality (VR) as a tool for sensorimotor training opens a window for creating otherwise impossible sensory experiences and sensorimotor interactions. Specifically, we studied how VR adaptation training in ecological conditions modulates spontaneous functional connectivity and brain representation of naturalistic real-life-like stimuli. Previous adaptation studies used artificial, lab-designed setups both during adaptation and while measuring subsequent aftereffects. Testing brain response while observing naturalistic stimuli and in resting state allowed us to stay as close as possible to naturalistic real-life-like conditions, not confounded by performance during a task. The current work demonstrates how rapid changes in free-flowing brain activity and connectivity occur following short-term VR visuomotor adaptation training in healthy individuals. Moreover, we found a link between sensory responses to naturalistic stimuli and adaptation-induced behavioural aftereffect, thus demonstrating a common source of training-induced spatial recalibration, which affects both behaviour and brain representations of naturalistic stimuli. These findings might have meaningful implications both for understanding the mechanisms underlying visuomotor plasticity in healthy individuals and for using VR adaptation training as a tool for rehabilitating brain-damaged patients suffering from deficits in spatial representation.
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During NREM sleep hippocampal Sharp-wave ripples (SWR) events are thought to stabilize memory traces for long-term storage in downstream neocortical structures. Within the neocortex, Default Mode Network (DMN) areas interact preferentially with the hippocampus purportedly to consolidate those traces. Transient bouts of slow oscillations and sleep spindles in DMN areas are often observed around SWRs, suggesting that these two activities are related and that their interplay possibly contributes to memory consolidation. To investigate how SWRs interact with the DMN and spindles, we combined cortical wide-field voltage imaging, ECoG, and hippocampal LFP recordings in anesthetized and sleeping mice. Here we show that, during SWR, ″up-states″ and spindles reliably co-occur in a cortical subnetwork centered around the Retrosplenial cortex. Furthermore, Retrosplenial transient activations and spindles predict Slow Gamma oscillations in CA1 during SWRs. Together, our results suggest that Retrosplenial-hippocampal interaction may be a central source of information exchange between cortex and hippocampus.
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Neutral events preceding emotional experiences can be better remembered, likely by assigning them as significant to guide possible use in future. Yet, the neurobiological mechanisms of how emotional learning enhances memory for past mundane events remain unclear. By two behavioral studies and one functional magnetic resonance imaging study with an adapted sensory preconditioning paradigm, we show rapid neural reactivation and connectivity changes underlying emotion-charged retroactive memory enhancement. Behaviorally, emotional learning enhanced initial memory for neutral associations across the three studies. Neurally, emotional learning potentiated trial-specific reactivation of overlapping neural traces in the hippocampus and stimulus-relevant neocortex. It further induced rapid hippocampal-neocortical functional reorganization supporting such retroactive memory benefit, as characterized by enhanced hippocampal-neocortical coupling modulated by the amygdala during emotional learning, and a shift of hippocampal connectivity from stimulus-relevant neocortex to transmodal prefrontal-parietal areas at post-learning rests. Together, emotional learning retroactively promotes memory integration for past neutral events through stimulating trial-specific reactivation of overlapping representations and reorganization of associated memories into an integrated network to foster its priority for future use.
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Older adults exhibit deficits in episodic memory tasks, which have often been attributed to encoding or retrieval deficits, with little attention to consolidation mechanisms. More recently, researchers have attempted to measure consolidation in the context of a behavioral experiment using the wakeful rest paradigm (i.e., a brief, quiet period of minimal stimulation, which facilitates memory performance, compared to a distractor task). Critically, older adults might not produce this effect, given established age differences in other episodic memory processes and mind-wandering. In three experiments, we directly compared younger and older adults in modified versions of the wakeful rest paradigm. Critically, we utilized incidental encoding procedures (all experiments) and abstract shape stimuli (in Experiment 3) to limit the possibility of retrieval practice or maintenance rehearsal as potential confounding mechanisms in producing the wakeful rest effect. Wakeful rest reliably and equally benefited recall of incidentally encoded words in both younger and older adults. In contrast, wakeful rest had no benefit for standard accuracy measures of recognition performance in verbal stimuli, although there was an effect in response latencies for non-verbal stimuli. Overall, these results suggest that the benefits of wakeful rest on episodic retrieval are preserved across age groups, and hence support age-independence in potential consolidation mechanisms as measured by wakeful rest. Further, these benefits do not appear to be dependent on the intentionality of encoding or variations in distractor task types. Finally, the lack of wakeful rest benefits on recognition performance might be driven by theoretical constraints on the effect or methodological limitations of recognition memory testing in the current paradigm.
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Systems consolidation theories propose two mechanisms that enable the behavioral integration of related memories: coordinated reactivation between hippocampus and cortex, and the emergence of cortical traces that reflect overlap across memories. However, there is limited empirical evidence that links these mechanisms to the emergence of behavioral integration over time. In two experiments, participants implicitly encoded sequences of objects with overlapping structure. Assessment of behavioral integration showed that response times during a recognition task reflected behavioral priming between objects that never occurred together in time but belonged to overlapping sequences. This priming was consolidation-dependent and only emerged for sequences learned 24 hours prior to the test. Critically, behavioral integration was related to changes in neural pattern similarity in the medial prefrontal cortex and increases in post-learning rest connectivity between the posterior hippocampus and lateral occipital cortex. These findings suggest that memories with a shared predictive structure become behaviorally and neurally integrated through a consolidation-related restructuring of the learned sequences, providing insight into the relationship between different consolidation mechanisms that support behavioral integration.
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Memory consolidation is the process in which memory traces are strengthened over time for later retrieval. Although some theories hold that consolidation can only occur during sleep, accumulating evidence suggests that brief periods of wakeful rest may also facilitate consolidation. Interestingly, however, Varma and colleagues reported that a demanding 2-back task following encoding produced a similar performance to a wakeful reset condition. We tested whether participants’ recall would be best following a wakeful rest condition as compared to other distractor conditions, consistent with the extant wakeful rest literature, or whether we would replicate the finding by Varma and colleagues such that participants’ memory benefitted from both a rest and a 2-back task following encoding. Across two experiments, we used similar (Experiment 1) and the same (Experiment 2) encoding material as used the one by Varma and colleagues, employed a wakeful rest condition adapted for online testing, and compared participants’ recall across post-encoding conditions. In the first experiment, we used a between-subjects design and compared participants’ cued recall performance following a period of wakeful rest, a 2-back task, or a rest + sounds condition. The second experiment more closely replicated the experimental design used by Varma and colleagues using a within-subjects manipulation. Ultimately, our findings more consistently aligned with the canonical wakeful rest finding, such that recall was better following the rest condition than all other post-encoding conditions. These results support the notion that wakeful rest may allow for consolidation by protecting recently encoded information from interference, thereby improving memory performance.
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Systems consolidation of new experiences into lasting episodic memories involves hippocampal–neocortical interactions. Evidence of this process is already observed during early post-encoding rest periods, both as increased hippocampal coupling with task-relevant perceptual regions and reactivation of stimulus-specific patterns following intensive encoding tasks. We investigate the spatial and temporal characteristics of these hippocampally anchored post-encoding neocortical modulations. Eighty-nine adults participated in an experiment consisting of interleaved memory task- and resting-state periods. We observed increased post-encoding functional connectivity between hippocampus and individually localized neocortical regions responsive to stimuli encountered during memory encoding. Post-encoding modulations were manifested as a nearly system-wide upregulation in hippocampal coupling with all major functional networks. The configuration of these extensive modulations resembled hippocampal–neocortical interaction patterns estimated from active encoding operations, suggesting hippocampal post-encoding involvement exceeds perceptual aspects. Reinstatement of encoding patterns was not observed in resting-state scans collected 12 h later, nor when using other candidate seed regions. The similarity in hippocampal functional coupling between online memory encoding and offline post-encoding rest suggests reactivation in humans involves a spectrum of cognitive processes engaged during the experience of an event. There were no age effects, suggesting that upregulation of hippocampal–neocortical connectivity represents a general phenomenon seen across the adult lifespan.
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Cognitive Reserve (CR) refers to the preservation of cognitive function in the face of age- or disease-related neuroanatomical decline. While bilingualism is known to contribute to CR, the extent to which, and what particular aspect of, second language experience contributes to CR are debated, and the underlying neural mechanism(s) unknown. Intrinsic functional connectivity reflects experience-dependent neuroplasticity that occurs across timescales ranging from minutes to decades, and may be a neural mechanism underlying CR. To test this hypothesis, we used voxel-based morphometry and resting-state functional connectivity analyses of MRI data to compare structural and functional brain integrity between bilingual and monolingual older adults, matched on cognitive performance using a rigorous propensity score matching technique, and across levels of second language proficiency measured as a continuous variable. Bilingualism, and degree of second language proficiency in particular, were associated with lower grey matter integrity in a hub of the default mode network, a region that is particularly vulnerable to decline in aging and dementia, but preserved functional network organization that resembled the young adult brain. Our findings confirm that lifelong bilingualism contributes to CR through experience-dependent maintenance of optimal functional network structure of the domain-general attentional control network across the lifespan.
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Memory consolidation is a continuous transformative process between encoding and retrieval of mental representations. Recent research has shown that neural activity immediately after encoding is particularly associated with later successful retrieval. It is currently unclear whether post-encoding neural activity makes a distinct and causal contribution to memory consolidation. Here, we investigated the role of the post-encoding period for consolidation of spatial memory in neurologically normal human subjects. We used the GABAA-ergic anesthetic propofol to transiently manipulate neural activity during the initial stage of spatial memory consolidation without affecting encoding or retrieval. A total of 52 participants undergoing minor surgery learned to navigate to a target in a five-armed maze derived from animal experiments. Participants completed learning either immediately prior to injection of propofol (early group) or more than 60 minutes before injection (late group). Four hours after anesthesia, participants were tested for memory-guided navigation. Our results show a selective impairment of navigation in the early group and near-normal performance in the late group. Analysis of navigational error patterns further suggested that propofol impaired distinct aspects of spatial representations, in particular sequences of path segments and spatial relationships between landmarks. We conclude that neural activity during the post-encoding period makes a causal and specific contribution to consolidation of representations underlying self-centered and world-centered memory-guided navigation. Distinct aspects of these representations are susceptible to GABAA-ergic modulation within a post-encoding time-window of less than 60 minutes, presumably reflecting associative processes that contribute to the formation of integrated spatial representations that guide future behavior.
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Connectivity of the brain at rest can reflect individual differences and impact behavioral outcomes, including memory. The present study investigated how culture influences functional connectivity with regions of the medial temporal lobe. In this study, 46 Americans and 59 East Asians completed a resting state scan after encoding pictures of objects. To investigate cross-cultural differences in resting state functional connectivity, left parahippocampal gyrus (anterior and posterior regions) and left hippocampus were selected as seed regions. These regions were selected, because they were previously implicated in a study of cultural differences during the successful encoding of detailed memories. Results revealed that left posterior parahippocampal gyrus had stronger connectivity with temporo-occipital regions for East Asians compared with Americans and stronger connectivity with parieto-occipital regions for Americans compared with East Asians. Left anterior parahippocampal gyrus had stronger connectivity with temporal regions for East Asians than Americans and stronger connectivity with frontal regions for Americans than East Asians. Although connectivity did not relate to memory performance, patterns did relate to cultural values. The degree of independent self-construal and subjective value of tradition were associated with functional connectivity involving left anterior parahippocampal gyrus. Findings are discussed in terms of potential cultural differences in memory consolidation or more general trait or state-based processes, such as holistic versus analytic processing.
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Propofol is well known to cause amnesia independent of its sedative effect. Memory consolidation processes in the hippocampus have been proposed as a target — however the neural substrates for propofol’s amnesic actions remain understudied and poorly described. In particular, the potential role of the cerebral cortex has not been investigated. As an in vitro experimental model of cortical memory consolidation, potentiated cerebral cortex evoked responses were generated in mouse neocortical slices using high frequency (20 Hz) stimulation to layer IV cortical grey matter or subcortical white matter. In separate experiments, slices were pretreated with propofol at two concentrations, 2 µg/mL and 4 µg/mL, to determine the effect of clinically relevant propofol levels on the potentiation response. Only grey matter stimulation induced a significant and lasting increase in cortical evoked potential amplitude in the drug-free condition. Propofol at 2 µg/mL completely inhibited cortical evoked response potentiation, while the 4 µg/mL concentration caused a small but significant depressant effect consequent to the high frequency stimulation. These findings support the hypothesis that propofol disrupts memory consolidation and actively facilitates memory decay in the cerebral cortex. The results further highlight the importance of the the cerebral cortex in the early phase of long term memory consolidation.
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Experiencing stress before an event can influence how that event is later remembered. In the current study, we examine how individual differences in one’s physiological response to a stressor is related to changes to underlying brain states and memory performance. Specifically, we examined how changes in intrinsic amygdala connectivity relate to positive and negative memory performance as a function of stress response, defined as a change in cortisol. Twenty‐five participants underwent a social stressor before an incidental emotional memory encoding task. Cortisol samples were obtained before and after the stressor to measure individual differences in stress response. Three resting state scans (pre‐stressor, post‐stressor/pre‐encoding, and post‐encoding) were conducted to evaluate pre‐ to post‐stressor and pre‐ to post‐encoding changes to intrinsic amygdala connectivity. Analyses examined relations between greater cortisol changes and connectivity changes. Greater cortisol increases were associated with a greater decrease in prefrontal‐amygdala connectivity following the stressor and a reversal in the relation between prefrontal‐amygdala connectivity and negative vs. positive memory performance. Greater cortisol increases were also associated with a greater increase in amygdala connectivity with a number of posterior sensory regions following encoding. Consistent with prior findings in non‐stressed individuals, pre‐ to post‐encoding increases in amygdala‐posterior connectivity were associated with greater negative relative to positive memory performance, although this was specific to lateral rather than medial posterior regions and to participants with the greatest cortisol changes. These findings suggest that stress response is associated with changes in intrinsic connectivity that have downstream effects on the valence of remembered emotional content.
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Spontaneous neural activity in human as assessed with resting-state functional magnetic resonance imaging (fMRI) exhibits brain-wide coordinated patterns in the frequency of <0.1 Hz. However, understanding of fast brain-wide networks at the timescales of neuronal events (milliseconds to sub-seconds) and their spatial, spectral, and transitional characteristics remain limited due to the temporal constraints of hemodynamic signals. With milli-second resolution and whole-head coverage, scalp-based electroencephalography (EEG) provides a unique window into brain-wide networks with neuronal-timescale dynamics, shedding light on the organizing principles of brain functions. Using the state-of-the-art signal processing techniques, we reconstructed cortical neural tomography from resting-state EEG and extracted component-based co-activation patterns (cCAPs). These cCAPs revealed brain-wide intrinsic networks and their dynamics, indicating the configuration/reconfiguration of resting human brains into recurring and transitional functional states, which are featured with the prominent spatial phenomena of global patterns and anti-state pairs of co-(de)activations. Rich oscillational structures across a wide frequency band (i.e., 0.6 Hz, 5 Hz, and 10 Hz) were embedded in the nonstationary dynamics of these functional states. We further identified a superstructure that regulated between-state immediate and long-range transitions involving the entire set of identified cCAPs and governed a significant aspect of brain-wide network dynamics. These findings demonstrated how resting-state EEG data can be functionally decomposed using cCAPs to reveal rich dynamic structures of brain-wide human neural activations.
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Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and cortical systems - both during and after encoding. Developmental changes in these distributed neural circuits may lead to age-related differences in reward-motivated memory and the underlying neural mechanisms. Converging evidence from cross-species studies suggests that subcortical dopamine signaling is increased during adolescence, which may lead to stronger memory representations of rewarding, relative to mundane, events and changes in the contributions of underlying subcortical and cortical brain mechanisms across age. Here, we used fMRI to examine how reward motivation influences the "online" encoding and "offline" post-encoding brain mechanisms that support long-term associative memory from childhood to adulthood in human participants of both sexes. We found that reward motivation led to both age-invariant enhancements and nonlinear age-related differences in associative memory after 24 hours. Furthermore, reward-related memory benefits were linked to age-varying neural mechanisms. During encoding, interactions between the prefrontal cortex and ventral tegmental area (VTA) were associated with better high-reward memory to a greater degree with increasing age. Pre- to post-encoding changes in functional connectivity between the anterior hippocampus and VTA were also associated with better high-reward memory, but more so at younger ages. Our findings suggest that there may be developmental differences in the contributions of offline subcortical and online cortical brain mechanisms supporting reward-motivated memory.SIGNIFICANCE STATEMENTA substantial body of research has examined the neural mechanisms through which reward influences memory formation in adults. However, despite extensive evidence that both reward processing and associative memory undergo dynamic change across development, few studies have examined age-related changes in these processes. We found both age-invariant and nonlinear age-related differences in reward-motivated memory. Moreover, our findings point to developmental differences in the processes through which reward modulates the prioritization of information in long-term memory - with greater early reliance on offline subcortical consolidation mechanisms and increased contribution of systems-level online encoding circuitry with increasing age. These results highlight dynamic developmental changes in the cognitive and neural mechanisms through which motivationally salient information is prioritized in memory from childhood to adulthood.
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Background: Oxytocin is the current domestic first-line agent of induced labor and labor augmentation, and its potential effects on neonatal neurobehavioral development is currently attracting increased attention. Objective: To explore the effect of different doses of synOT on neonatal instinctive breastfeeding behavior and breastfeeding by observing neonatal behaviors during SSC with mothers after delivery. Methods: A total of 154 pairs of pregnant women and their newborns were selected by random sampling. Observations and comparisons of neonatal instinctive behaviors were conducted by using the Widström's 9 Stages method.According to the dosage of oxytocin, subjects were divided into a low dose group (2.5 U) of 39 pairs, a medium dose group (≥ 5 U) of 38 pairs, a high dose group (≥ 10 U) of 38 pairs and a control group (no synOT use) of 39 couples. The occurrence time of newborns' instinctive movements and the duration time of each behavior stage for the four groups were also analyzed.The frequency of exclusive breastfeeding within 3 days after birth and the rate of exclusive breastfeeding at 3 months were collected and compared. Results: The intrapartum administration of synthetic oxytocin affects the expression of neonatal instinctive breastfeeding. With increases in drug dose, the effect of breast seeking activity and breast attachment will be more significant, and the effect of oxytocin on sucking and breastfeeding was dose-dependent. Conclusions: Intrapartum exposure to the different doses of synOT could affect the neonatal instinctive behaviors during skin-to-skin contact within two hours after birth to varying degrees, there were also adverse effects on the initiation and continuation of postpartum breastfeeding, with dose-dependent results.
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Learning results from online (within-session) and offline (between-sessions) changes. Heterogeneity of age-related effects in learning may be ascribed to aging differentially affecting these two processes. We investigated the contribution of online and offline consolidation in visuo-spatial working memory (vWM). Younger and older participants performed a vWM task on day one and after nine days, allowing us to disentangle online and offline learning effects. To test whether offline consolidation needs continuous practice, two additional groups of younger and older adults performed the same vWM task in between the two assessments. Similarly to other cognitive domains, older adults improved vWM through online (during session one) but not through offline learning. Practice was necessary to improve vWM between sessions in older participants. Younger adults instead exhibited only offline improvement, regardless of practice. The findings suggest that while online learning remains efficient in aging, practice is instead required to support more fragile offline mechanisms.
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Background It is gradually becoming clear that obsessive-compulsive disorder (OCD) patients have aberrant resting-state large-scale intrinsic networks of cingulo-opercular salience (SN), default mode (DMN), and front-parietal network (FPN). However, it remains unknown whether unaffected first-degree relatives of OCD patients have these alterations as a vulnerability marker to the disorder. Methods We performed resting-state functional magnetic resonance imaging (rsfMRI) scans of 47 medication-free OCD patients, 21 unaffected healthy first-degree relatives of OCD patients, and 62 healthy control (HC) participants. We explored differences between the three groups in the functional connectivity from SN (seeds: anterior-insula (AI) and dorsal anterior cingulate cortex (dACC)), DMN (seeds: medial prefrontal cortex (MPFC) and posterior parietal cortex (PCC)), and FPN (seeds: dorsolateral prefrontal cortex (DLPFC)). Results Compared to HC, both OCD patients and first-degree relatives showed significantly greater functional connectivity between AI and PCC and between DLPFC and the thalamus. Compared to first-degree relatives and HC, OCD patients showed reduced functional connectivity between PCC and DLPFC. Conclusions OCD patients and unaffected first-degree relatives of OCD patients showed overlapping alterations in resting state functional connectivity between the regions of SN and DMN and between DLPFC and the thalamus. Our results suggested that alterations between large-scale intrinsic networks and within the dorsal cognitive cortico-striato-thalamo-cortical (CSTC) circuit could represent endophenotype markers of OCD.
Chapter
Neuro-plasticity describes the ability of the brain in achieving novel functions, either by transforming its internal connectivity, or by changing the elements of which it is made, meaning that, only those changes, that affect both structural and functional aspects of the system, can be defined as “plastic.” The concept of plasticity can be applied to molecular as well as to environmental events that can be recognized as the basic mechanism by which our brain reacts to the internal and external stimuli. When considering brain plasticity within a clinical context–that is the process linked with changes of brain functions following a lesion- the term “reorganization” is somewhat synonymous, referring to the specific types of structural/functional modifications observed as axonal sprouting, long-term synaptic potentiation/inhibition or to the plasticity related genomic responses. Furthermore, brain rewires during maturation, and aging thus maintaining a remarkable learning capacity, allowing it to acquire a wide range of skills, from motor actions to complex abstract reasoning, in a lifelong expression. In this review, the contribution on the “neuroplasticity” topic coming from advanced analysis of EEG rhythms is put forward.
Chapter
In higher education, the focus of teachers is almost always on content delivery and less so the process of learning, an issue exacerbated in the rise of online courses that are often treated as receptacles for content. As a result, college success often depends on strategies that are rarely communicated, leading to inequitable learning outcomes. Fortunately, principles from the field of cognitive psychology about how the brain learns best are increasingly being applied to the classroom, bringing a focus on the process of learning for all students. Four principles of particular interest in this chapter are retrieval practice (practice remembering), spacing of learning episodes, interleaving of related topics, and elaboration of material. Tips for implementing these principles in the online classroom will also be discussed. When teachers shift the focus from content delivery to how students learn, equitable learning is supported.
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Systems consolidation of new experiences into lasting episodic memories involves interactions between hippocampus and the neocortex. Evidence of this process is seen already during early awake post-encoding rest periods. Functional MRI (fMRI) studies have demonstrated increased hippocampal coupling with task-relevant perceptual regions and reactivation of stimulus-specific encoding patterns following intensive encoding tasks. Here we investigate the spatial and temporal characteristics of these hippocampally anchored post-encoding neocortical modulations. Eighty-nine adults participated in an experiment consisting of interleaved memory task- and resting-state periods. As expected, we observed increased post-encoding functional connectivity between hippocampus and individually localized neocortical regions responsive to stimulus categories encountered during memory encoding. Post-encoding modulations were however not restricted to stimulus-selective cortex, but manifested as a nearly system-wide upregulation in hippocampal coupling with all major functional networks. The spatial configuration of these extensive modulations resembled hippocampal-neocortical interaction patterns estimated from active encoding operations, suggesting hippocampal post-encoding involvement by far exceeds reactivation of perceptual aspects. This reinstatement of encoding patterns during immediate post-encoding rest was not observed in resting-state scans collected 12 hours later, nor in control analyses estimating post-encoding neocortical modulations in functional connectivity using other candidate seed regions. The broad similarity in hippocampal functional coupling between online memory encoding and offline post-encoding rest suggests reactivation in humans may involve a spectrum of cognitive processes engaged during experience of an event. Significance statement Stabilization of newly acquired information into lasting memories occurs through systems consolidation – a process which gradually spreads the locus of memory traces from hippocampus to more distributed neocortical representations. One of the earliest signs of consolidation is the upregulation of hippocampal-neocortical interactions during periods of awake rest following an active encoding task. We here show that these modulations involve much larger parts of the brain than previously reported in humans. Comparing changes in hippocampal coupling during post-encoding rest with those observed under active encoding, we find evidence for encoding-like hippocampal reinstatement throughout cortex during task-free periods. This suggests early systems consolidation of an experience involves reactivating not only core sensory details but multiple additional aspects of the encoding event.
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Recent studies have suggested that resting-state brain functional connectivity (RSFC) has the potential to discriminate among individuals in a population. These studies mostly utilized a pattern of RSFC obtained from one scan to identify a given individual from the set of patterns obtained from the second scan. However, it remains unclear whether the discriminative ability would change with the extension of the time span between the two brain scans. This study explores the variations in the discriminative ability of RSFC on eight time spans, including 6 hours, 12 hours, 1 day, 1 month, 3-6 months, 7-12 months, 1-2 years and 2-3 years. We first searched for a set of the most discriminative RSFCs using the data of 200 healthy adult subjects from the Human Connectome Project dataset, and we then utilized this set of RSFCs to identify individuals from a population. The variations in the discriminative accuracies over different time spans were evaluated on datasets from a total of 682 unseen adult subjects acquired from four different sites. We found that although the accuracies were detectable at above-chance levels, the discriminative accuracies showed a significant decrease (F=17.87, p<0.01) along with the extension of brain imaging time span, from over 90% within one month to 66% at 2-3 years. Furthermore, the decreasing trend was robust and not dependent on the training set or analysis method. Therefore, we suggest that the discriminative ability of RSFC in identifying individuals should be susceptible to the length of time between brain scans.
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The human brain demonstrates complex yet systematic patterns of neural activity at rest. We examined whether functional connectivity among those brain regions typically active during rest depends on ongoing and recent task demands and individual differences. We probed the temporal coordination among these regions during periods of language comprehension and during the rest periods that followed comprehension. Our findings show that the topography of this "rest network" varies with exogenous processing demands. The network encompassed more highly interconnected regions during rest than during listening, but also when listening to unsurprising vs. surprising information. Furthermore, connectivity patterns during rest varied as a function of recent listening experience. Individual variability in connectivity strength was associated with cognitive function: more attentive comprehenders demonstrated weaker connectivity during language comprehension, and a greater differentiation between connectivity during comprehension and rest. The regions we examined have generally been thought to form an invariant physiological and functional network whose activity reflects spontaneous cognitive processes. Our findings suggest that their function extends beyond the mediation of unconstrained thought, and that they play an important role in higher-level cognitive function.
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Sharp wave-ripple (SPW-R) complexes in the hippocampus-entorhinal cortex are believed to be important for transferring labile memories from the hippocampus to the neocortex for long-term storage. We found that selective elimination of SPW-Rs during post-training consolidation periods resulted in performance impairment in rats trained on a hippocampus-dependent spatial memory task. Our results provide evidence for a prominent role of hippocampal SPW-Rs in memory consolidation.
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Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.
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Slow-wave sleep (SWS) is important for memory consolidation. During sleep, neural patterns reflecting previously acquired information are replayed. One possible reason for this is that such replay exchanges information between hippocampus and neocortex, supporting consolidation. We recorded neuron ensembles in the rat medial prefrontal cortex (mPFC) to study memory trace reactivation during SWS following learning and execution of cross-modal strategy shifts. In general, reactivation of learning-related patterns occurred in distinct, highly synchronized transient bouts, mostly simultaneous with hippocampal sharp wave/ripple complexes (SPWRs), when hippocampal ensemble reactivation and cortico-hippocampal interaction is enhanced. During sleep following learning of a new rule, mPFC neural patterns that appeared during response selection replayed prominently, coincident with hippocampal SPWRs. This was learning dependent, as the patterns appeared only after rule acquisition. Therefore, learning, or the resulting reliable reward, influenced which patterns were most strongly encoded and successively reactivated in the hippocampal/prefrontal network.
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Functionally related brain networks are engaged even in the absence of an overt behavior. The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2-4]) or electrical [5, 6] signals, is unclear. Two major proposals are that resting state activity supports introspective thought or supports responses to future events [7]. An alternative perspective is that the resting brain actively and selectively processes previous experiences [8]. Here we show that motor learning can modulate subsequent activity within resting networks. BOLD signal was recorded during rest periods before and after an 11 min visuomotor training session. Motor learning but not motor performance modulated a fronto-parietal resting state network (RSN). Along with the fronto-parietal network, a cerebellar network not previously reported as an RSN was also specifically altered by learning. Both of these networks are engaged during learning of similar visuomotor tasks [9-22]. Thus, we provide the first description of the modulation of specific RSNs by prior learning--but not by prior performance--revealing a novel connection between the neuroplastic mechanisms of learning and resting state activity. Our approach may provide a powerful tool for exploration of the systems involved in memory consolidation.
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Incoming events that match or mismatch stored representations are thought to influence the ability of the hippocampus to switch between memory encoding and retrieval modes. Electrophysiological work has dissociated match and mismatch signals in the monkey perirhinal cortex, where match signals were selective for matches to goal states, whereas mismatch signals were not modulated by intention (Miller and Desimone, 1994). To investigate whether the theoretically important relational match and mismatch signals in the hippocampus are modulated by goal states, we fully crossed whether a probe stimulus relationally matched or mismatched a previously perceived image or goal state. Subjects performed two working memory tasks in which they either responded "yes" to probes that were identical to the previous sample scene or, after performing a relational manipulation of the scene, responded "yes" only to a probe that was identical to this perceptually novel image. Using functional magnetic resonance imaging, we found evidence for relational match enhancements bilaterally in the hippocampus that were selective for matches between the probe stimulus and goal state, but were not modulated by whether that goal was perceptually novel. Moreover, we found evidence for a complementary hippocampal mismatch enhancement that was triggered by stimuli containing salient perceptual manipulations. Our results provided evidence for parallel memory signatures in the hippocampus: a controlled match signal that can detect matches to internally generated goal states and an automatic mismatch signal that can identify unpredicted perceptual novelty.
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Human beings differ in their ability to form and retrieve lasting long-term memories. To explore the source of these individual differences, we used functional magnetic resonance imaging to measure blood-oxygen-level-dependent (BOLD) activity in healthy young adults (n = 50) during periods of resting fixation that were interleaved with periods of simple cognitive tasks. We report that medial temporal lobe BOLD activity during periods of rest predicts individual differences in memory ability. Specifically, individuals who exhibited greater magnitudes of task-induced deactivations in medial temporal lobe BOLD signal (as compared to periods of rest) demonstrated superior memory during offline testing. This relationship was independent of differences in general cognitive function and persisted across different control tasks (i.e., number judgment versus checkerboard detection) and experimental designs (i.e., blocked versus event-related). These results offer a neurophysiological basis for the variability in mnemonic ability that is present amongst healthy young adults and may help to guide strategies aimed at early detection and intervention of neurological and mnemonic impairment. • default network • fMRI • hippocampus • individual differences • resting-activity
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Episodic and spatial memories engage the hippocampus during acquisition but migrate to the cerebral cortex over time. We have recently proposed that the interplay between slow-wave (SWS) and rapid eye movement (REM) sleep propagates recent synaptic changes from the hippocampus to the cortex. To test this theory, we jointly assessed extracellular neuronal activity, local field potentials (LFP), and expression levels of plasticity-related immediate-early genes (IEG) arc and zif-268 in rats exposed to novel spatio-tactile experience. Post-experience firing rate increases were strongest in SWS and lasted much longer in the cortex (hours) than in the hippocampus (minutes). During REM sleep, firing rates showed strong temporal dependence across brain areas: cortical activation during experience predicted hippocampal activity in the first post-experience hour, while hippocampal activation during experience predicted cortical activity in the third post-experience hour. Four hours after experience, IEG expression was specifically upregulated during REM sleep in the cortex, but not in the hippocampus. Arc gene expression in the cortex was proportional to LFP amplitude in the spindle-range (10-14 Hz) but not to firing rates, as expected from signals more related to dendritic input than to somatic output. The results indicate that hippocampo-cortical activation during waking is followed by multiple waves of cortical plasticity as full sleep cycles recur. The absence of equivalent changes in the hippocampus may explain its mnemonic disengagement over time.
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Damage to the hippocampal system disrupts recent memory but leaves remote memory intact. The account presented here suggests that memories are first stored via synaptic changes in the hippocampal system, that these changes support reinstatement of recent memories in the neocortex, that neocortical synapses change a little on each reinstatement, and that remote memory is based on accumulated neocortical changes. Models that learn via changes to connections help explain this organization. These models discover the structure in ensembles of items if learning of each item is gradual and interleaved with learning about other items. This suggests that the neocortex learns slowly to discover the structure in ensembles of experiences. The hippocampal system permits rapid learning of new items without disrupting this structure, and reinstatement of new memories interleaves them with others to integrate them into structured neocortical memory systems.
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The stages of integration leading from local feature analysis to object recognition were explored in human visual cortex by using the technique of functional magnetic resonance imaging. Here we report evidence for object-related activation. Such activation was located at the lateral-posterior aspect of the occipital lobe, just abutting the posterior aspect of the motion-sensitive area MT/V5, in a region termed the lateral occipital complex (LO). LO showed preferential activation to images of objects, compared to a wide range of texture patterns. This activation was not caused by a global difference in the Fourier spatial frequency content of objects versus texture images, since object images produced enhanced LO activation compared to textures matched in power spectra but randomized in phase. The preferential activation to objects also could not be explained by different patterns of eye movements: similar levels of activation were observed when subjects fixated on the objects and when they scanned the objects with their eyes. Additional manipulations such as spatial frequency filtering and a 4-fold change in visual size did not affect LO activation. These results suggest that the enhanced responses to objects were not a manifestation of low-level visual processing. A striking demonstration that activity in LO is uniquely correlated to object detectability was produced by the "Lincoln" illusion, in which blurring of objects digitized into large blocks paradoxically increases their recognizability. Such blurring led to significant enhancement of LO activation. Despite the preferential activation to objects, LO did not seem to be involved in the final, "semantic," stages of the recognition process. Thus, objects varying widely in their recognizability (e.g., famous faces, common objects, and unfamiliar three-dimensional abstract sculptures) activated it to a similar degree. These results are thus evidence for an intermediate link in the chain of processing stages leading to object recognition in human visual cortex.
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A fundamental question about human memory is why some experiences are remembered whereas others are forgotten. Brain activation during word encoding was measured using blocked and event-related functional magnetic resonance imaging to examine how neural activation differs for subsequently remembered and subsequently forgotten experiences. Results revealed that the ability to later remember a verbal experience is predicted by the magnitude of activation in left prefrontal and temporal cortices during that experience. These findings provide direct evidence that left prefrontal and temporal regions jointly promote memory formation for verbalizable events.
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Information in neuronal networks may be represented by the spatiotemporal patterns of spikes. Here we examined the temporal coordination of pyramidal cell spikes in the rat hippocampus during slow-wave sleep. In addition, rats were trained to run in a defined position in space (running wheel) to activate a selected group of pyramidal cells. A template-matching method and a joint probability map method were used for sequence search. Repeating spike sequences in excess of chance occurrence were examined by comparing the number of repeating sequences in the original spike trains and in surrogate trains after Monte Carlo shuffling of the spikes. Four different shuffling procedures were used to control for the population dynamics of hippocampal neurons. Repeating spike sequences in the recorded cell assemblies were present in both the awake and sleeping animal in excess of what might be predicted by random variations. Spike sequences observed during wheel running were "replayed" at a faster timescale during single sharp-wave bursts of slow-wave sleep. We hypothesize that the endogenously expressed spike sequences during sleep reflect reactivation of the circuitry modified by previous experience. Reactivation of acquired sequences may serve to consolidate information.
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During active behavior, patterns of hippocampal and neocortical neuronal activity reflect ongoing inputs and their contexts. Recent neurophysiological investigations have shown that during 'off-line' periods, traces of these experiences are spontaneously reactivated in both structures. Although the functional importance of this phenomenon remains to be demonstrated, it does provide clues about the nature and mechanisms of memory retrieval and consolidation.
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Hippocampal-neocortical interactions in memory have typically been characterized within the "standard model" of memory consolidation. In this view, memory storage initially requires hippocampal linking of dispersed neocortical storage sites, but over time this need dissipates, and the hippocampal component is rendered unnecessary. This change in function over time is held to account for the retrograde amnesia (RA) gradients often seen in patients with hippocampal damage. Recent evidence, however, calls this standard model into question, and we have recently proposed a new approach, the "multiple memory trace" (MMT) theory. In this view, hippocampal ensembles are always involved in storage and retrieval of episodic information, but semantic (gist) information can be established in neocortex, and will survive damage to the hippocampal system if enough time has elapsed. This approach accounts more readily for the very long RA gradients often observed in amnesia. We report the results of analytic and connectionist simulations that demonstrate the feasibility of MMT. We also report a neuroimaging study showing that retrieval of very remote (25-year-old) memories elicits as much activation in hippocampus as retrieval of quite recent memories. Finally, we report new data from the study of patients with temporal lobe damage, using more sensitive measures than previously the case, showing that deficits in both episodic and spatial detail can be observed even for very remote memories. Overall, these findings indicate that the standard model of memory consolidation, which views the hippocampus as having only a temporary role in memory, is wrong. Instead, the data support the view that for episodic and spatial detail the hippocampal system is always necessary.
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A baseline or control state is fundamental to the understanding of most complex systems. Defining a baseline state in the human brain, arguably our most complex system, poses a particular challenge. Many suspect that left unconstrained, its activity will vary unpredictably. Despite this prediction we identify a baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF. The OEF is defined as the ratio of oxygen used by the brain to oxygen delivered by flowing blood and is remarkably uniform in the awake but resting state (e.g., lying quietly with eyes closed). Local deviations in the OEF represent the physiological basis of signals of changes in neuronal activity obtained with functional MRI during a wide variety of human behaviors. We used quantitative metabolic and circulatory measurements from positron-emission tomography to obtain the OEF regionally throughout the brain. Areas of activation were conspicuous by their absence. All significant deviations from the mean hemisphere OEF were increases, signifying deactivations, and resided almost exclusively in the visual system. Defining the baseline state of an area in this manner attaches meaning to a group of areas that consistently exhibit decreases from this baseline, during a wide variety of goal-directed behaviors monitored with positron-emission tomography and functional MRI. These decreases suggest the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
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The precise contribution of perirhinal cortex to human episodic memory is uncertain. Human intracranial recordings highlight a role in successful episodic memory encoding, but encoding-related perirhinal activation has not been observed with functional imaging. By adapting functional magnetic resonance imaging scanning parameters to maximize sensitivity to medial temporal lobe activity, we demonstrate that left perirhinal and hippocampal responses during word list encoding are greater for subsequently recalled than forgotten words. Although perirhinal responses predict memory for all words, successful encoding of initial words in a list, demonstrating a primacy effect, is associated with parahippocampal and anterior hippocampal activation. We conclude that perirhinal cortex and hippocampus participate in successful memory encoding. Encoding-related parahippocampal and anterior hippocampal responses for initial, remembered words most likely reflects enhanced attentional orienting to these positionally distinctive items.
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Declarative memory consolidation is enhanced by sleep. In the investigation of underlying mechanisms, mainly rapid eye movement (REM) sleep and slow-wave sleep have been considered. More recently, sleep stage 2 with sleep spindles as a most prominent feature has received increasing attention. Specifically, in rats hippocampal ripples were found to occur in temporal proximity to cortical sleep spindles, indicating an information transfer between the hippocampus and neocortex, which is supposed to underlie the consolidation of declarative memories during sleep. This study in humans looks at the changes in EEG activity during nocturnal sleep after extensive training on a declarative learning task, as compared with a nonlearning control task of equal visual stimulation and subjectively rated cognitive strain. Time spent in each sleep stage, spindle density, and EEG power spectra for 28 electrode locations were determined. During sleep after training, the density of sleep spindles was significantly higher after the learning task as compared with the nonlearning control task. This effect was largest during the first 90 min of sleep (p < 0.01). Additionally, spindle density was correlated to recall performance both before and after sleep (r = 0.56; p < 0.05). Power spectra and time spent in sleep stages did not differ between learning and nonlearning conditions. Results indicate that spindle activity during non-REM sleep is sensitive to previous learning experience.
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The integrity of the hippocampus and surrounding medial-temporal cortices is critical for episodic memory, with the hippocampus being posited to support relational or configural associative learning. The present event-related functional magnetic resonance imaging (fMRI) study investigated the role of specific medial-temporal lobe structures in learning during relational and item-based processing, as well as the extent to which these structures are engaged during item-based maintenance of stimuli in working memory. fMRI indexed involvement of the hippocampus and underlying cortical regions during performance of two verbal encoding conditions, one that required item-based maintenance of word triplets in working memory and the other that entailed the formation of inter-item associations across the words in each triplet. Sixteen subjects were scanned using a rapid event-related fMRI design while they encountered the item-based and relational processing trials. To examine the correlation between fMRI signal in medial-temporal structures during learning and the subject's subsequent ability to remember the stimuli (a measure of effective memory formation), subjects were administered a yes-no recognition memory test following completion of the encoding scans. Results revealed that the hippocampus proper was engaged during both relational and item-based processing, with relational processing resulting in a greater hippocampal response. By contrast, entorhinal and parahippocampal gyri were differentially engaged during item-based processing, providing strong evidence for a functional neuroanatomic distinction between hippocampal and parahippocampal structures. Analysis of the neural correlates of subsequent memory revealed that activation in the bilateral hippocampus was reliably correlated with behavioral measures of effective memory formation only for those stimuli that were encoded in a relational manner. Taken together, these data provide evidence that the hippocampus, while engaged during item-based working memory maintenance, differentially subserves the relational binding of items into an integrated memory trace so that the experience can be later remembered.
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Conversion of new memories into a lasting form may involve the gradual refinement and linking together of neural representations stored widely throughout neocortex. This consolidation process may require coordinated reactivation of distributed components of memory traces while the cortex is “offline,” i.e., not engaged in processing external stimuli. Simultaneous neural ensemble recordings from four sites in the macaque neocortex revealed such coordinated reactivation. In motor, somatosensory, and parietal cortex (but not prefrontal cortex), the behaviorally induced correlation structure and temporal patterning of neural ensembles within and between regions were preserved, confirming a major tenet of the trace-reactivation theory of memory consolidation.
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