Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies

The present study performed a quantitative meta-analysis of functional MRI studies that used a subsequent memory approach. The meta-analysis considered both subsequent memory (SM; remembered>forgotten) and subsequent forgetting (SF; forgotten>remembered) effects, restricting the data used to that concerning visual information encoding in healthy young adults. The meta-analysis of SM effects indicated that they most consistently associated with five neural regions: left inferior frontal cortex (IFC), bilateral fusiform cortex, bilateral hippocampal formation, bilateral premotor cortex (PMC), and bilateral posterior parietal cortex (PPC). Direct comparisons of the SM effects between the studies using verbal versus pictorial material and item-memory versus associative-memory tasks yielded three main sets of findings. First, the left IFC exhibited greater SM effects during verbal material than pictorial material encoding, whereas the fusiform cortex exhibited greater SM effects during pictorial material rather than verbal material encoding. Second, bilateral hippocampal regions showed greater SM effects during pictorial material encoding compared to verbal material encoding. Furthermore, the left hippocampal region showed greater SM effects during pictorial-associative versus pictorial-item encoding. Third, bilateral PMC and PPC regions, which may support attention during encoding, exhibited greater SM effects during item encoding than during associative encoding. The meta-analysis of SF effects indicated they associated mostly with default-mode network regions, including the anterior and posterior midline cortex, the bilateral temporoparietal junction, and the bilateral superior frontal cortex. Recurrent activity oscillations between the task-positive and task-negative/default-mode networks may account for trial-to-trial variability in participants' encoding performances, which is a fundamental source of both SM and SF effects. Taken together, these findings clarify the neural activity that supports successful encoding, as well as the neural activity that leads to encoding failure.

[1]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

[2]  Andrew P. Yonelinas,et al.  Perirhinal Cortex Supports Encoding and Familiarity-Based Recognition of Novel Associations , 2008, Neuron.

[3]  J. Desmond,et al.  Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. , 2001, Brain : a journal of neurology.

[4]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[5]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[6]  Ken A Paller,et al.  Neural Evidence That Vivid Imagining Can Lead to False Remembering , 2004, Psychological science.

[7]  Daniel L. Schacter,et al.  How Negative Emotion Enhances the Visual Specificity of a Memory , 2007, Journal of Cognitive Neuroscience.

[8]  S. Petersen,et al.  Frontal cortex contributes to human memory formation , 1999, Nature Neuroscience.

[9]  Elizabeth A. Kensinger,et al.  What Neural Correlates Underlie Successful Encoding and Retrieval? A Functional Magnetic Resonance Imaging Study Using a Divided Attention Paradigm , 2003, The Journal of Neuroscience.

[10]  Jason P. Mitchell,et al.  Feeling-of-knowing in episodic memory: an event-related fMRI study , 2003, NeuroImage.

[11]  I. Tendolkar,et al.  Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level , 2001, Brain Research Bulletin.

[12]  R. Henson A Mini-Review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[13]  Michael D. Rugg,et al.  Dissociation of the neural correlates of visual and auditory contextual encoding , 2010, Neuropsychologia.

[14]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[15]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[16]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[17]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[18]  Paul C. Fletcher,et al.  Regional Brain Activations Predicting Subsequent Memory Success: An Event-Related Fmri Study of the Influence of Encoding Tasks , 2003, Cortex.

[19]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[20]  C. Elger,et al.  Temporal and cerebellar brain regions that support both declarative memory formation and retrieval. , 2004, Cerebral cortex.

[21]  Robert M. Siwiec,et al.  Neural Correlates of Successful Encoding Identified Using Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[22]  Jing Luo,et al.  Dissecting medial temporal lobe contributions to item and associative memory formation , 2009, NeuroImage.

[23]  Kerry Lee,et al.  Recognition memory for studied words is determined by cortical activation differences at encoding but not during retrieval , 2004, NeuroImage.

[24]  K. Paller,et al.  Observing the transformation of experience into memory , 2002, Trends in Cognitive Sciences.

[25]  Yoko Mano,et al.  Dissociable Roles of the Anterior Temporal Regions in Successful Encoding of Memory for Person Identity Information , 2010, Journal of Cognitive Neuroscience.

[26]  V. S. Reed,et al.  Pictorial superiority effect. , 1976, Journal of experimental psychology. Human learning and memory.

[27]  John D E Gabrieli,et al.  Neural correlates of actual and predicted memory formation , 2005, Nature Neuroscience.

[28]  Michael D Rugg,et al.  Encoding and the Durability of Episodic Memory: A Functional Magnetic Resonance Imaging Study , 2005, The Journal of Neuroscience.

[29]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[30]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  John T Wixted,et al.  Activity in the Medial Temporal Lobe Predicts Memory Strength, Whereas Activity in the Prefrontal Cortex Predicts Recollection , 2008, The Journal of Neuroscience.

[32]  Charan Ranganath,et al.  Prefrontal Cortex and Long-Term Memory Encoding: An Integrative Review of Findings from Neuropsychology and Neuroimaging , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[33]  Melina R. Uncapher,et al.  Selecting for Memory? The Influence of Selective Attention on the Mnemonic Binding of Contextual Information , 2009, The Journal of Neuroscience.

[34]  Lila Davachi,et al.  Behavioral / Systems / Cognitive Differential Encoding Mechanisms for Subsequent Associative Recognition and Free Recall , 2012 .

[35]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[36]  M. Forsting,et al.  Neural Encoding Correlates of High and Low Verbal Memory Performance , 2006 .

[37]  Philippe Fossati,et al.  Modulation of Memory Formation by Stimulus Content: Specific Role of the Medial Prefrontal Cortex in the Successful Encoding of Social Pictures , 2007, Journal of Cognitive Neuroscience.

[38]  Klaus Fliessbach,et al.  The effect of word concreteness on recognition memory , 2006, NeuroImage.

[39]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[40]  G. Northoff,et al.  Rest-stimulus interaction in the brain: a review , 2010, Trends in Neurosciences.

[41]  Marcia K. Johnson,et al.  Neuroimaging a Single Thought: Dorsolateral PFC Activity Associated with Refreshing Just-Activated Information , 2002, NeuroImage.

[42]  Tobias Sommer,et al.  Hippocampal–prefrontal encoding activation predicts whether words can be successfully recalled or only recognized , 2006, Behavioural Brain Research.

[43]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[44]  R. Cabeza,et al.  Handbook of functional neuroimaging of cognition , 2001 .

[45]  D. Schacter,et al.  The neural origins of specific and general memory: the role of the fusiform cortex , 2005, Neuropsychologia.

[46]  M. Rugg,et al.  Task-dependency of the neural correlates of episodic encoding as measured by fMRI. , 2001, Cerebral cortex.

[47]  J. Gläscher,et al.  Dissociable contributions within the medial temporal lobe to encoding of object-location associations. , 2005, Learning & memory.

[48]  Angela R. Laird,et al.  Lost in localization? The focus is meta-analysis , 2009, NeuroImage.

[49]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[50]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[51]  Daniel L Schacter,et al.  Encoding activity in anterior medial temporal lobe supports subsequent associative recognition , 2004, NeuroImage.

[52]  R. Henson,et al.  State-related and item-related neural correlates of successful memory encoding , 2002, Nature Neuroscience.

[53]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[54]  Randy L. Buckner,et al.  Encoding Processes during Retrieval Tasks , 2001, Journal of Cognitive Neuroscience.

[55]  H. Heinze,et al.  Reward-Related fMRI Activation of Dopaminergic Midbrain Is Associated with Enhanced Hippocampus- Dependent Long-Term Memory Formation , 2005, Neuron.

[56]  F. Craik,et al.  The effects of divided attention on encoding and retrieval processes in human memory. , 1996, Journal of experimental psychology. General.

[57]  Mahzarin R. Banaji,et al.  Encoding-Specific Effects of Social Cognition on the Neural Correlates of Subsequent Memory , 2004, The Journal of Neuroscience.

[58]  A M Dale,et al.  Prefrontal‐hippocampal‐fusiform activity during encoding predicts intraindividual differences in free recall ability: An event‐related functional‐anatomic MRI study , 2007, Hippocampus.

[59]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[60]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[61]  R. Malach,et al.  Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems , 2008, Neuropsychologia.

[62]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[63]  Simon Finnigan,et al.  fMRI evidence of word frequency and strength effects during episodic memory encoding. , 2005, Brain research. Cognitive brain research.

[64]  Guillén Fernández,et al.  Probing the neural correlates of associative memory formation: A parametrically analyzed event-related functional MRI study , 2007, Brain Research.

[65]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[66]  Hans-Jochen Heinze,et al.  Neuroanatomical Dissociation of Encoding Processes Related to Priming and Explicit Memory , 2006, The Journal of Neuroscience.

[67]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[68]  Rajita Sinha,et al.  Greater activation of the “default” brain regions predicts stop signal errors , 2007, NeuroImage.

[69]  H. Heinze,et al.  Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation , 2005 .

[70]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[71]  R. Cabeza,et al.  Effects of aging on the neural correlates of successful item and source memory encoding. , 2008, Journal of experimental psychology. Learning, memory, and cognition.

[72]  Steven Graham,et al.  Word frequency and subsequent memory effects studied using event-related fMRI , 2003, NeuroImage.

[73]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[74]  M. Rugg,et al.  Fractionation of the component processes underlying successful episodic encoding: A combined fmri and divided-attention study , 2008 .

[75]  R. Cabeza,et al.  Differential contributions of prefrontal, medial temporal, and sensory-perceptual regions to true and false memory formation. , 2007, Cerebral cortex.

[76]  Jeffrey R. Binder,et al.  Interrupting the “stream of consciousness”: An fMRI investigation , 2006, NeuroImage.

[77]  Jane F. Banfield,et al.  Medial prefrontal activity predicts memory for self. , 2004, Cerebral cortex.

[78]  Robert C. Welsh,et al.  Aging and the Neural Correlates of Successful Picture Encoding: Frontal Activations Compensate for Decreased Medial-Temporal Activity , 2005, Journal of Cognitive Neuroscience.

[79]  M. Rugg,et al.  When more means less neural activity related to unsuccessful memory encoding , 2001, Current Biology.

[80]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

[81]  Arthur P. Wunderlich,et al.  Emotional context modulates subsequent memory effect , 2003, NeuroImage.

[82]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[83]  Russell A. Poldrack,et al.  Putting names to faces: Successful encoding of associative memories activates the anterior hippocampal formation , 2003, NeuroImage.

[84]  M. Boly,et al.  Baseline brain activity fluctuations predict somatosensory perception in humans , 2007, Proceedings of the National Academy of Sciences.

[85]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

[86]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[87]  M. Chun,et al.  Linking Implicit and Explicit Memory: Common Encoding Factors and Shared Representations , 2006, Neuron.

[88]  Melina R. Uncapher,et al.  Episodic Encoding Is More than the Sum of Its Parts: An fMRI Investigation of Multifeatural Contextual Encoding , 2006, Neuron.

[89]  Barry Dainton,et al.  Stream of Consciousness , 2000, Tragedy of the Commons (Poetry).

[90]  Christian Büchel,et al.  Contributions of occipital, parietal and parahippocampal cortex to encoding of object-location associations , 2005, Neuropsychologia.

[91]  J. G. Snodgrass,et al.  The picture superiority effect: support for the distinctiveness model. , 1999, The American journal of psychology.

[92]  L. Otten,et al.  Fragments of a larger whole: retrieval cues constrain observed neural correlates of memory encoding. , 2007, Cerebral cortex.

[93]  Roberto Cabeza,et al.  Overlapping brain activity between episodic memory encoding and retrieval: Roles of the task-positive and task-negative networks , 2010, NeuroImage.

[94]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[95]  R. Sperling,et al.  Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation , 2008, Proceedings of the National Academy of Sciences.

[96]  R. Buckner,et al.  Neural correlates of verbal memory encoding during semantic and structural processing tasks , 2001, Neuroreport.

[97]  R. Habib,et al.  Neural correlates of availability and accessibility in memory. , 2008, Cerebral cortex.

[98]  Takashi Tsukiura,et al.  Distinguishing the Neural Correlates of Episodic Memory Encoding and Semantic Memory Retrieval , 2007, Psychological science.

[99]  L. Nyberg,et al.  Brain activation while forming memories of fearful and neutral faces in women and men. , 2007, Emotion.

[100]  Klaus Fliessbach,et al.  Cerebellar contributions to episodic memory encoding as revealed by fMRI , 2007, NeuroImage.

[101]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[102]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[103]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[104]  Anthony D Wagner,et al.  Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control , 2003, Neuropsychologia.

[105]  M. Rugg,et al.  The relationship between aging, performance, and the neural correlates of successful memory encoding. , 2009, Cerebral cortex.

[106]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[107]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[108]  Ramona O Hopkins,et al.  Item memory, source memory, and the medial temporal lobe: concordant findings from fMRI and memory-impaired patients. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[109]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

[110]  A. Yonelinas Recognition memory ROCs for item and associative information: The contribution of recollection and familiarity , 1997, Memory & cognition.

[111]  Nancy Kanwisher,et al.  Functional Neuroimaging of Visual Recognition , 2001 .

[112]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[113]  J. Desmond,et al.  Material‐specific lateralization of prefrontal activation during episodic encoding and retrieval , 1998, Neuroreport.

[114]  D. Montaldi,et al.  Object priming and recognition memory: Dissociable effects in left frontal cortex at encoding , 2009, Neuropsychologia.

[115]  Anthony D Wagner,et al.  Conceptual and perceptual novelty effects in human medial temporal cortex , 2005, Hippocampus.

[116]  John D E Gabrieli,et al.  Working memory and long‐term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes , 2006, Hippocampus.

[117]  S. M. Daselaar,et al.  When less means more: deactivations during encoding that predict subsequent memory , 2004, NeuroImage.

[118]  Michael D. Rugg,et al.  Further Dissociating the Processes Involved in Recognition Memory: An fMRI Study , 2005, Journal of Cognitive Neuroscience.

[119]  Henrik Walter,et al.  Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition , 2005, NeuroImage.

[120]  Martin Lepage,et al.  A face to remember: emotional expression modulates prefrontal activity during memory formation , 2005, NeuroImage.

[121]  Anthony D. Wagner,et al.  Posterior parietal cortex and episodic encoding: Insights from fMRI subsequent memory effects and dual-attention theory , 2009, Neurobiology of Learning and Memory.

[122]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[123]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[124]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[125]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[126]  R. Cabeza,et al.  Effects of aging on transient and sustained successful memory encoding activity , 2007, Neurobiology of Aging.

[127]  Alex Martin,et al.  Automatic activation of the medial temporal lobe during encoding: Lateralized influences of meaning and novelty , 1999, Hippocampus.

[128]  R. Clark,et al.  Recognition memory and the medial temporal lobe: a new perspective , 2007, Nature Reviews Neuroscience.

[129]  Heekyeong Park,et al.  Effects of study task on the neural correlates of source encoding. , 2008, Learning & memory.

[130]  L. Davachi,et al.  Cognitive neuroscience: Forgetting of things past , 2001, Current Biology.

[131]  Nikolai Axmacher,et al.  Interaction of working memory and long-term memory in the medial temporal lobe. , 2008, Cerebral cortex.

[132]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[133]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[134]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[135]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[136]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[137]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[138]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[139]  J. Buhle,et al.  Typologies of attentional networks , 2006, Nature Reviews Neuroscience.

[140]  Guillén Fernández,et al.  Probing the transformation of discontinuous associations into episodic memory: An event-related fMRI study , 2007, NeuroImage.

[141]  K. Norman,et al.  Memory Strength and Repetition Suppression: Multimodal Imaging of Medial Temporal Cortical Contributions to Recognition , 2005, Neuron.

[142]  M. Lindquist,et al.  Meta-analysis of functional neuroimaging data: current and future directions. , 2007, Social cognitive and affective neuroscience.

[143]  Richard S. J. Frackowiak,et al.  Age effects on the neural correlates of successful memory encoding. , 2003, Brain : a journal of neurology.

[145]  Yael Shrager,et al.  Activity in Both Hippocampus and Perirhinal Cortex Predicts the Memory Strength of Subsequently Remembered Information , 2008, Neuron.

[146]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[147]  Heekyeong Park,et al.  Neural correlates of successful encoding of semantically and phonologically mediated inter-item associations , 2008, NeuroImage.