Dissociable roles of default-mode regions during episodic encoding

We investigated the role of distinct regions of the default-mode network (DMN) during memory encoding with fMRI. Subjects encoded words using either a strategy that emphasized self-referential (pleasantness) processing, or one that emphasized semantic (man-made/natural) processing. During encoding subjects were intermittently presented with thought probes to evaluate if they were concentrated and on-task or exhibiting task-unrelated thoughts (TUT). After the scanning session subjects performed a source retrieval task to determine which of two judgments they performed for each word at encoding. Source retrieval accuracy was higher for words encoded with the pleasantness vs. the man-made/natural task and there was a trend for higher performance for words preceding on-task vs. TUT reports. fMRI results show that left anterior medial PFC and left angular gyrus activity was greater during successful vs. unsuccessful encoding during both encoding tasks. Greater activity in left anterior cingulate and bilateral lateral temporal cortex was related successful vs. unsuccessful encoding only in the pleasantness task. In contrast, posterior cingulate, right anterior cingulate and right temporoparietal junction were activated to a greater extent in unsuccessful vs. successful encoding across tasks. Finally, activation in posterior cingulate and bilateral dorsolateral prefrontal cortex was related to TUT across tasks; moreover, we observed a conjunction in posterior cingulate between encoding failure and TUT. We conclude that DMN regions play dissociable roles during memory formation, and that their association with subsequent memory may depend on the manner in which information is encoded and retrieved.

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

[2]  Audrey Duarte,et al.  Medial prefrontal cortex supports source memory accuracy for self-referenced items , 2012, Social neuroscience.

[3]  J. Morris,et al.  Functional deactivations: Change with age and dementia of the Alzheimer type , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Blair T. Johnson,et al.  The self-reference effect in memory: a meta-analysis. , 1997, Psychological bulletin.

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

[6]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[7]  Beatriz Luna,et al.  Combining Brains: A Survey of Methods for Statistical Pooling of Information , 2002, NeuroImage.

[8]  Alana T. Wong,et al.  Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration , 2007, Neuropsychologia.

[9]  Georg Northoff,et al.  How is our self related to midline regions and the default-mode network? , 2011, NeuroImage.

[10]  R. Buckner,et al.  Evidence for the Default Network's Role in Spontaneous Cognition , 2010 .

[11]  Steve Majerus,et al.  Neural Correlates of Ongoing Conscious Experience: Both Task-Unrelatedness and Stimulus-Independence Are Related to Default Network Activity , 2011, PloS one.

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

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

[14]  Jeffrey D. Johnson,et al.  Encoding-retrieval overlap in human episodic memory: a functional neuroimaging perspective. , 2008, Progress in brain research.

[15]  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.

[16]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[17]  E. Tulving,et al.  Network Analysis of Positron Emission Tomography Regional Cerebral Blood Flow Data: Ensemble Inhibition during Episodic Memory Retrieval , 1996, The Journal of Neuroscience.

[18]  Hongkeun Kim,et al.  A dual-subsystem model of the brain's default network: Self-referential processing, memory retrieval processes, and autobiographical memory retrieval , 2012, NeuroImage.

[19]  H. Ellis,et al.  Irrelevant thoughts, emotional mood states, and cognitive task performance , 1991, Memory & cognition.

[20]  Cheryl L. Grady,et al.  The default network and processing of personally relevant information: Converging evidence from task-related modulations and functional connectivity , 2010, Neuropsychologia.

[21]  Demis Hassabis,et al.  The construction system of the brain , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  John D. Bransford,et al.  Levels of processing versus transfer appropriate processing , 1977 .

[23]  P. Ruby,et al.  What is self-specific? Theoretical investigation and critical review of neuroimaging results. , 2009, Psychological review.

[24]  Endel Tulving,et al.  Encoding specificity and retrieval processes in episodic memory. , 1973 .

[25]  S. M. Daselaar,et al.  Explaining the encoding/retrieval flip: Memory-related deactivations and activations in the posteromedial cortex , 2012, Neuropsychologia.

[26]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[27]  Steven E. Prince,et al.  Encoding and retrieving faces and places: Distinguishing process- and stimulus-specific differences in brain activity , 2009, Neuropsychologia.

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

[29]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[30]  M. Rajah,et al.  Age-related changes in frequency of mind-wandering and task-related interferences during memory encoding and their impact on retrieval , 2013, Memory.

[31]  Niall W. Duncan,et al.  Anterior cingulate activity and the self in disorders of consciousness , 2010, Human Brain Mapping.

[32]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[33]  R. Cabeza,et al.  Posterior Midline and Ventral Parietal Activity is Associated with Retrieval Success and Encoding Failure , 2009, Front. Hum. Neurosci..

[34]  J. Smallwood,et al.  Task unrelated thought whilst encoding information , 2003, Consciousness and Cognition.

[35]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[36]  Martin Walter,et al.  The role of hippocampus dysfunction in deficient memory encoding and positive symptoms in schizophrenia , 2010, Psychiatry Research: Neuroimaging.

[37]  R. Nathan Spreng,et al.  The Fallacy of a “Task-Negative” Network , 2012, Front. Psychology.

[38]  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.

[39]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[40]  T. B. Rogers,et al.  Self-reference and the encoding of personal information. , 1977, Journal of personality and social psychology.

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

[42]  John W. Tukey,et al.  Statistical Methods for Research Workers , 1930, Nature.

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

[44]  J. Smallwood,et al.  The restless mind. , 2006, Psychological bulletin.

[45]  Alain Desrochers,et al.  Subjective frequency and imageability ratings for 3,600 French nouns , 2009, Behavior research methods.

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

[47]  J. Cummings,et al.  The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment , 2005, Journal of the American Geriatrics Society.

[48]  Paul C. Fletcher,et al.  Anterior prefrontal cortex and the recollection of contextual information , 2005, Neuropsychologia.

[49]  Hongkeun Kim,et al.  Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies , 2011, NeuroImage.

[50]  C. Grady,et al.  Age differences in default and reward networks during processing of personally relevant information , 2012, Neuropsychologia.

[51]  M. Rajah,et al.  Age-related changes in the three-way correlation between anterior hippocampus volume, whole-brain patterns of encoding activity and subsequent context retrieval , 2011, Brain Research.

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

[53]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[54]  Michael R. Dulas,et al.  The effects of aging on material-independent and material-dependent neural correlates of contextual binding , 2011, NeuroImage.

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

[56]  M. Kendall Statistical Methods for Research Workers , 1937, Nature.

[57]  H. Walter,et al.  The relationship between level of processing and hippocampal–cortical functional connectivity during episodic memory formation in humans , 2013, Human brain mapping.

[58]  Marcia K. Johnson,et al.  Source monitoring. , 1993, Psychological bulletin.