Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences
NeuronPublished 1 January 2010Open access
Arielle Tambini, Nicholas Ketz, Lila Davachi
Citations623
SJR quartileQ1
SJR score6.75
SNIP2.95
Generate an AI Snapshot to get a quick, structured summary of this paper.
Study Snapshot
ObjectiveStudy objective
MethodsResearch methodology
PopulationPopulation studied
Sample sizeSample sizes
OutcomesStudy outcomes here
ResultsStudy results comes here
LimitationsResearch study limitations comes here
A concise AI-generated summary of the paper will appear here once you click Generate AI Snapshot.
TL;DR
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, and the magnitude of hippocampal-LO correlations during posttask rest predicts individual differences in later associative memory.
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.
Keywords
Neuroscience
Proceedings of the National Academy of SciencesA default mode of brain function
12,398 Citations2001Marcus E. Raichle, Ann Mary MacLeod +4 more
A baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF is identified, suggesting the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
Proceedings of the National Academy of SciencesThe human brain is intrinsically organized into dynamic, anticorrelated functional networks
8,846 Citations2005Michael Fox, Abraham Z. Snyder +4 more
It is suggested that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain, featuring the presence of anticorrelated networks in the absence of overt task performance.
Journal of NeuroscienceThe Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception
7,943 Citations1997Nancy Kanwisher, Josh H. McDermott +1 more
The data allow us to reject alternative accounts of the function of the fusiform face area (area “FF”) that appeal to visual attention, subordinate-level classification, or general processing of any animate or human forms, demonstrating that this region is selectively involved in the perception of faces.
Nature reviews. NeuroscienceSpontaneous fluctuations in brain activity observed with functional magnetic resonance imaging
6,881 Citations2007Michael Fox, Marcus E. Raichle
Recent studies examining spontaneous fluctuations in the blood oxygen level dependent (BOLD) signal of functional magnetic resonance imaging as a potentially important and revealing manifestation of spontaneous neuronal activity are reviewed.
Proceedings of the National Academy of SciencesFunctional connectivity in the resting brain: A network analysis of the default mode hypothesis
6,509 Citations2002Michael D. Greicius, Ben Krasnow +2 more
This study constitutes, to the knowledge, the first resting-state connectivity analysis of the default mode and provides the most compelling evidence to date for the existence of a cohesive default mode network.
International Journal of Computer VisionModeling the Shape of the Scene: A Holistic Representation of the Spatial Envelope
6,410 Citations2001Aude Oliva, Antonio Torralba
The performance of the spatial envelope model shows that specific information about object shape or identity is not a requirement for scene categorization and that modeling a holistic representation of the scene informs about its probable semantic category.
Psychological ReviewWhy there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory.
5,355 Citations1995James L. McClelland, Bruce L. McNaughton +1 more
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 neocorticals changes.
Psychological BulletinTests for comparing elements of a correlation matrix.
4,421 Citations1980James H. Steiger
Proceedings of the National Academy of SciencesConsistent resting-state networks across healthy subjects
4,400 Citations2006Jessica S. Damoiseaux, Serge A.R.B. Rombouts +5 more
Findings show that the baseline activity of the brain is consistent across subjects exhibiting significant temporal dynamics, with percentage BOLD signal change comparable with the signal changes found in task-related experiments.
ScienceReactivation of Hippocampal Ensemble Memories During Sleep
3,195 Citations1994Matthew A. Wilson, Bruce L. McNaughton
Recordings from large ensembles of hippocampal "place cells" in three rats showed that cells that fired together when the animal occupied particular locations in the environment exhibited an increased tendency to fire together during subsequent sleep, in comparison to sleep episodes preceding the behavioral tasks.
NatureA cortical representation of the local visual environment
3,112 Citations1998Russell A. Epstein, Nancy Kanwisher
Evidence is presented that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment, and it is proposed that the PPA represents places by encoding the geometry of the local environment.
Philosophical transactions of the Royal Society of London. Series B, Biological sciencesSimple memory: a theory for archicortex
2,808 Citations1971David Marr
It is shown that rather general numerical constraints roughly determine the dimensions of memorizing models for the mammalian brain, and from these is derived a general model for archicortex.
Trends in Cognitive SciencesSelf-projection and the brain
2,679 Citations2006Randy L. Buckner, Daniel Carroll
Proceedings of the National Academy of SciencesSpontaneous neuronal activity distinguishes human dorsal and ventral attention systems
2,162 Citations2006Michael Fox, Maurizio Corbetta +3 more
It is demonstrated that the neuroanatomical substrates of human attention persist in the absence of external events, reflected in the correlation structure of spontaneous activity.
Proceedings of the National Academy of SciencesObject-related activity revealed by functional magnetic resonance imaging in human occipital cortex.
1,818 Citations1995Rafael Malach, J.B. Reppas +8 more
Evidence for an intermediate link in the chain of processing stages leading to object recognition in human visual cortex is reported, which suggests that the enhanced responses to objects were not a manifestation of low-level visual processing.
NatureReverse replay of behavioural sequences in hippocampal place cells during the awake state
1,796 Citations2006David J. Foster, Matthew A. Wilson
It is reported that sequential replay occurs in the rat hippocampus during awake periods immediately after spatial experience, which has a unique form, in which recent episodes of spatial experience are replayed in a temporally reversed order.
Nature NeuroscienceCoordinated memory replay in the visual cortex and hippocampus during sleep
1,752 Citations2006Daoyun Ji, Matthew Wilson
It is found that spiking patterns not only in the cortex but also in the hippocampus were organized into frames, defined as periods of stepwise increase in neuronal population activity.
ScienceBuilding Memories: Remembering and Forgetting of Verbal Experiences as Predicted by Brain Activity
1,657 Citations1998Anthony D. Wagner, Daniel L. Schacter +6 more
Findings provide direct evidence that left prefrontal and temporal regions jointly promote memory formation for verbalizable events.
Nature NeuroscienceSelective suppression of hippocampal ripples impairs spatial memory
1,595 Citations2009Gabrielle Girardeau, Karim Benchenane +3 more
It is 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, providing evidence for a prominent role of hippocampal SPW -Rs in memory consolidation.
Vision ResearchThe lateral occipital complex and its role in object recognition
1,482 Citations2001Kalanit Grill‐Spector, Zoe Kourtzi +1 more
Overall, these results indicate that the lateral occipital complex plays an important role in human object recognition.
PubMedFrequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data.
1,454 Citations2001Dietmar Cordes, Victor M. Haughton +6 more
Functional connectivity in the auditory, visual, and sensorimotor cortices is characterized predominantly by frequencies slower than those in the cardiac and respiratory cycles, which are characterized by a high degree of temporal coherence.
NeuronMemory of Sequential Experience in the Hippocampus during Slow Wave Sleep
1,341 Citations2002Albert K. Lee, Matthew A. Wilson
Rats repeatedly ran through a sequence of spatial receptive fields of hippocampal CA1 place cells in a fixed temporal order, consistent with evidence that the hippocampus is crucial for spatial learning in rodents and the formation of long-term memories of events in time in humans.
Nature NeuroscienceForward and reverse hippocampal place-cell sequences during ripples
1,285 Citations2007Kamran Diba, György Buzsáki
It is reported that temporal spike sequences from hippocampal place neurons of rats on an elevated track recurred in reverse order at the end of a run, but in forward order in anticipation of the run, coinciding with sharp waves.
ScienceOdor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation
1,217 Citations2007Björn Rasch, Christian Büchel +2 more
It is shown that reactivation indeed causes memory consolidation during sleep, and functional magnetic resonance imaging revealed significant hippocampal activation in response to odor re-exposure during SWS.
Current Opinion in NeurobiologyItem, context and relational episodic encoding in humans
1,162 Citations2006Lila Davachi
Emerging findings demonstrate that thelevel of engagement of perirhinal cortex predicts later memory for individual items, whereas the level of hippocampal processing correlates with later relational memory, or recovery of additional episodic details, and provide emerging evidence for domain-specificity within the perirHinal and parahippocampal cortices.
ScienceMaking Memories: Brain Activity that Predicts How Well Visual Experience Will Be Remembered
1,114 Citations1998James B. Brewer, Zuo Zhao +3 more
Event-related functional magnetic resonance imaging was used to identify specific brain activations that differentiated between visual experiences that were later remembered well, remembered less well, or forgotten.
NeuronCoordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
1,082 Citations1998Athanassios G. Siapas, Matthew A Wilson
The existence of temporal correlations between hippocampal ripples and cortical spindles that are also reflected in the correlated activity of single neurons within these brain structures are demonstrated and may constitute an important mechanism of cortico-hippocampal communication during sleep.
Journal of NeurophysiologyCoherent Spontaneous Activity Identifies a Hippocampal-Parietal Memory Network
973 Citations2006Justin L. Vincent, Abraham Z. Snyder +5 more
Journal of NeuroscienceReplay and Time Compression of Recurring Spike Sequences in the Hippocampus
973 Citations1999Zoltán Nádasdy, Hajime Hirase +3 more
It is hypothesized that the endogenously expressed spike sequences during sleep reflect reactivation of the circuitry modified by previous experience and serve to consolidate information in neuronal networks.
Observed Brain Dynamics
911 Citations2007Partha P. Mitra, Hemant Bokil
This volume addresses the need for a textbook in this interdisciplinary area of neuroscience and is written for a broad spectrum of readers ranging from physical scientists, mathematicians, and statisticians wishing to educate themselves about neuroscience, to biologists who would like to learn time series analysis methods in particular and refresh their mathematical and statistical knowledge in general.
HippocampusDisruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat
872 Citations2009Valérie Ego‐Stengel, Matthew Wilson
It is shown that disrupting neuronal activity during ripple events impairs spatial learning in rats, and interfering with hippocampal processing during sleep led to decreased learning.
Journal of NeuroscienceLearning-Dependent Increases in Sleep Spindle Density
872 Citations2002Steffen Gais, Matthias Mölle +2 more
Results indicate that spindle activity during non-REM sleep is sensitive to previous learning experience, and spindle density was correlated to recall performance both before and after sleep.
Nature NeuroscienceAwake replay of remote experiences in the hippocampus
824 Citations2009Mattias Karlsson, Loren M. Frank
It is shown that stored representations are reactivated during both waking and sleep replay, and that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.
Nature NeuroscienceReplay of rule-learning related neural patterns in the prefrontal cortex during sleep
819 Citations2009Adrien Peyrache, Mehdi Khamassi +3 more
Recording neuron ensembles in the rat medial prefrontal cortex to study memory trace reactivation during SWS following learning and execution of cross-modal strategy shifts found that learning influenced which patterns were most strongly encoded and successively reactivated in the hippocampal/prefrontal network.
NeuronAre Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep?
758 Citations2004Philippe Peigneux, Steven Laureys +10 more
It is shown that, in humans, hippocampal areas that are activated during route learning in a virtual town are likewise activated during subsequent slow wave sleep, and that the amount of hippocampal activity expressed during slow waveSleep positively correlates with the improvement of performance in route retrieval on the next day.
Proceedings of the National Academy of SciencesWhen zero is not zero: The problem of ambiguous baseline conditions in fMRI
737 Citations2001Craig E.L. Stark, Larry R. Squire
It is demonstrated that periods of rest are associated with significant cognitive activity and provide a nonoptimal baseline for memory tasks and have important implications for the design and interpretation of a wide range of fMRI studies of cognition.
NeuroImageAnatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts
718 Citations1997Jeffrey G. Ojemann, Erbil Akbudak +4 more
Journal of NeuroscienceInfluences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes
691 Citations1989Constantine Pavlides, Jonathan Winson
The findings suggest that neuronal activity of hippocampal place cells in the awake states may influence the firing characteristics of these cells in subsequent sleep episodes, and increased firing rates along with the greater number of multiple spike bursts and the shorter interspike intervals within the burst, following exposure to a cell's place field, may represent possible information processing during sleep.
HippocampusMedial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval
663 Citations1999Daniel L. Schacter, Anthony D. Wagner
It is concluded that PET studies of encoding reveal both anterior and posterior MTL activations, more frequently than have fMRI studies, and possible sources of these differences are considered.
ScienceFast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
603 Citations2007David R. Euston, Masami Tatsuno +1 more
It is found that, during sleep, reactivation of spatiotemporal patterns was coherent across the network and compressed in time by a factor of 6 to 7.
Current BiologyThe Resting Human Brain and Motor Learning
531 Citations2009Neil B. Albert, Edwin M. Robertson +1 more
It is shown that motor learning can modulate subsequent activity within resting networks and is provided 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.
HippocampusMultiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results
519 Citations2000Lynn Nadel, Alexei V. Samsonovich +2 more
Overall, the data support the view that for episodic and spatial detail the hippocampal system is always necessary, and indicate that the standard model of memory consolidation, which views the hippocampus as having only a temporary role in memory, is wrong.
Journal of NeurophysiologyHippocampal Contributions to Episodic Encoding: Insights From Relational and Item-Based Learning
492 Citations2002Lila Davachi, Anthony D. Wagner
Evidence is provided 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.
ScienceCoordinated Reactivation of Distributed Memory Traces in Primate Neocortex
425 Citations2002Kari L. Hoffman, Bruce L. McNaughton
Simultaneous neural ensemble recordings from four sites in the macaque neocortex revealed that 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.
Neural ComputationSampling Properties of the Spectrum and Coherency of Sequences of Action Potentials
416 Citations2001M. R. Jarvis, Partha P. Mitra
The spectrum and coherency are useful quantities for characterizing the temporal correlations and functional relations within and between point processes and a known statistical test applies with little modification to point process spectra and is of utility in studying a point process driven by a continuous stimulus.
NeuroscienceOvernight verbal memory retention correlates with the number of sleep spindles
411 Citations2005Zsófia Clemens, Dániel Fabó +1 more
Current Opinion in NeurobiologyMemory trace reactivation in hippocampal and neocortical neuronal ensembles
381 Citations2000Gary R. Sutherland
Investigations have shown that during 'off-line' periods, traces of these experiences are spontaneously reactivated in hippocampal and neocortical neuronal activity, providing clues about the nature and mechanisms of memory retrieval and consolidation.
NeuropharmacologyThe late maintenance of hippocampal LTP: Requirements, phases, ‘synaptic tagging’, ‘late-associativity’ and implications
331 Citations2006Klaus G. Reymann, Julietta U. Frey
This group has shown that the induction of late-LTP requires the associative activation of heterosynaptic inputs, i.e. the synergistic activation of glutamatergic and modulatory, reinforcing inputs within specific, effective time windows.
Philosophical Transactions of the Royal Society B Biological SciencesMemory reprocessing in corticocortical and hippocampocortical neuronal ensembles
321 Citations1997Yulin Qin, Bruce L. McNaughton +2 more
Hippocampal cells that fire together during behaviour exhibit enhanced activity correlations during subsequent sleep, with some preservation of temporal order information, and traces of recent experience are re-expressed in both hippocampal and neocortical circuits during sleep.
NeuronNew Experiences Enhance Coordinated Neural Activity in the Hippocampus
303 Citations2008Sen Cheng, Loren M. Frank
It is shown that pairs of CA1 cells that represent overlapping novel locations are initially more coactive and more precisely coordinated than are cells representing overlapping familiar locations, which helps to induce synaptic plasticity and to allow for rapid storage of new memories.
NeuronState-Dependent Spike-Timing Relationships between Hippocampal and Prefrontal Circuits during Sleep
299 Citations2009Casimir M. Wierzynski, Evgueniy V. Lubenov +2 more
It is shown that cells in prefrontal cortex fire consistently within 100 ms after hippocampal cells in naturally sleeping animals, suggesting that SWR events are atomic units of hippocampal-prefrontal communication during SWS and that the coupling between these areas is highly attenuated during REM sleep.
Journal of Neuroscience MethodsNonparametric statistical testing of coherence differences
293 Citations2007Eric Maris, Jan‐Mathijs Schoffelen +1 more
It is shown that nonparametric statistical tests provide convincing and elegant solutions for both problems and allow to incorporate biophysically motivated constraints in the test statistic, which may drastically increase the sensitivity of the test.
NeuronHippocampal CA3 Output Is Crucial for Ripple-Associated Reactivation and Consolidation of Memory
293 Citations2009Toshiaki Nakashiba, Derek L. Buhl +2 more
It is found that posttraining blockade of CA3 output for up to 4 weeks impairs the consolidation of contextual fear memory and the posttraining integrity of the trisynaptic pathway and the ripple-associated reactivation of hippocampal memory engram are crucial for memory consolidation.
Learning & MemorySustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
275 Citations2008Oxana Eschenko, Wiâm Ramadan +3 more
These experiments show that the characteristics of hippocampal high-frequency oscillations during SWS are affected by prior behavioral experience, while Associative learning induces robust and sustained changes in several SPW-R characteristics.
PLoS BiologyLong-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas
275 Citations2004Sidarta Ribeiro, Damien Gervasoni +6 more
The results indicate that persistent experience-dependent neuronal reverberation is a general property of multiple forebrain structures, and does not consist of an exact replay of previous activity, but instead it defines a mild and consistent bias towards salient neural ensemble firing patterns.
PLoS BiologyOffline Persistence of Memory-Related Cerebral Activity during Active Wakefulness
267 Citations2006Philippe Peigneux, Pierre Orban +5 more
It is shown, using functional magnetic resonance imaging, that brain activity elicited during a new learning episode modulates brain responses to an unrelated cognitive task, during the waking period following the end of training.
Journal of NeuroscienceElevated Sleep Spindle Density after Learning or after Retrieval in Rats
256 Citations2006Oxana Eschenko, Matthias Mölle +2 more
The present study reports the first indication of learning-associated increase in spindle density in the rat, providing an animal model to study the role of brain oscillations in memory consolidation during sleep and substantially extend findings in humans.
Current Opinion in NeurobiologyMaintaining memories by reactivation
245 Citations2007Björn Rasch, Jan Born
It is proposed that memory reactivations during sleep are accompanied by a transient destabilization of memory traces, which allows for gradually adapting newly acquired memories to pre-existing long-term memories whereby invariants and certain other features of these memories become extracted.
Journal of NeuroscienceDissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding
226 Citations2002Bryan A. Strange, Leun J. Otten +3 more
Functional magnetic resonance imaging scanning parameters are adapted to maximize sensitivity to medial temporal lobe activity to demonstrate that left perirhinal and hippocampal responses during word list encoding are greater for subsequently recalled than forgotten words.
Proceedings of the National Academy of SciencesTask-dependent organization of brain regions active during rest
196 Citations2009Uri Hasson, Howard C. Nusbaum +1 more
The temporal coordination among these regions during periods of language comprehension and during the rest periods that followed comprehension was probed, showing that the topography of this “rest network” varies with exogenous processing demands.
Journal of Cognitive NeuroscienceWhen Keeping in Mind Supports Later Bringing to Mind: Neural Markers of Phonological Rehearsal Predict Subsequent Remembering
193 Citations2001Lila Davachi, Anat Maril +1 more
Contrary to the prevalent view that rote rehearsal does not impact learning, data suggest that phonological maintenance mechanisms, in addition to semantic elaboration, support the encoding of an experience such that it can be later remembered.
Cerebral CortexDissociation between Explicit Memory and Configural Memory in the Human Medial Temporal Lobe
139 Citations2008Alison R. Preston, John D. E. Gabrieli
Findings in functional magnetic resonance imaging indicate dissociable roles for hippocampus in learning that supports explicit recognition and for anterior MTL cortex in configural learning and converge with studies of amnesia.
Frontiers in NeuroscienceNovel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus
127 Citations2007Sidarta Ribeiro
The results indicate that hippocampo-cortical activation during waking is followed by multiple waves of cortical plasticity as full sleep cycles recur, and the absence of equivalent changes in the hippocampus may explain its mnemonic disengagement over time.
Journal of NeuroscienceMethodological Considerations on the Use of Template Matching to Study Long-Lasting Memory Trace Replay
91 Citations2006Masami Tatsuno, P. Lipa +1 more
These investigations indicate that the outcome of template-matching analysis is very sensitive to the conditions of how it is applied, and should be interpreted cautiously, and that the existence of long-lasting reverberation after a novel experience requires additional verification.
Journal of NeuroscienceDistinct Memory Signatures in the Hippocampus: Intentional States Distinguish Match and Mismatch Enhancement Signals
80 Citations2009Katherine Duncan, Clayton E. Curtis +1 more
Using functional magnetic resonance imaging, this work 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.
Proceedings of the National Academy of SciencesMedial temporal lobe BOLD activity at rest predicts individual differences in memory ability in healthy young adults
61 Citations2008Gagan S. Wig, Scott T. Grafton +4 more
It is reported that medial temporal lobe BOLD activity during periods of rest predicts individual differences in memory ability, which offers 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 andmnemonic impairment.