Detecting Representations of Recent and Remote Autobiographical Memories in vmPFC and Hippocampus

How autobiographical memories are represented in the human brain and whether this changes with time are questions central to memory neuroscience. Two regions in particular have been consistently implicated, the ventromedial prefrontal cortex (vmPFC) and the hippocampus, although their precise contributions are still contested. The key question in this debate, when reduced to its simplest form, concerns where information about specific autobiographical memories is located. Here, we availed ourselves of the opportunity afforded by multivoxel pattern analysis to provide an alternative to conventional neuropsychological and fMRI approaches, by detecting representations of individual autobiographical memories in patterns of fMRI activity. We examined whether information about specific recent (two weeks old) and remote (10 years old) autobiographical memories was represented in vmPFC and hippocampus, and other medial temporal and neocortical regions. vmPFC contained information about recent and remote autobiographical memories, although remote memories were more readily detected there, indicating that consolidation or a change of some kind had occurred. Information about both types of memory was also present in the hippocampus, suggesting it plays a role in the retrieval of vivid autobiographical memories regardless of remoteness. Interestingly, we also found that while recent and remote memories were both represented within anterior and posterior hippocampus, the latter nevertheless contained more information about remote memories. Thus, like vmPFC, the hippocampus too respected the distinction between recent and remote memories. Overall, these findings clarify and extend our view of vmPFC and hippocampus while also informing systems-level consolidation and providing clear targets for future studies.

[1]  Stephen C. Strother,et al.  Support vector machines for temporal classification of block design fMRI data , 2005, NeuroImage.

[2]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[4]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[5]  B Milner,et al.  Loss of recent memory after bilateral hippocampal lesions. 1957. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[6]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[7]  H. Duvernoy,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply , 1999 .

[8]  E. Maguire,et al.  Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients , 2012, Current Biology.

[9]  Brian Levine,et al.  The Effects of Rehearsal on the Functional Neuroanatomy of Episodic Autobiographical and Semantic Remembering: A Functional Magnetic Resonance Imaging Study , 2009, The Journal of Neuroscience.

[10]  F A Jolesz,et al.  Optimized single-slab three-dimensional spin-echo MR imaging of the brain. , 2000, Radiology.

[11]  Y. Dudai The restless engram: consolidations never end. , 2012, Annual review of neuroscience.

[12]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[13]  Morris Moscovitch,et al.  Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach , 2004, NeuroImage.

[14]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[15]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[16]  M. Hallett Human Brain Function , 1998, Trends in Neurosciences.

[17]  Robert Turner,et al.  Image Distortion Correction in fMRI: A Quantitative Evaluation , 2002, NeuroImage.

[18]  Valerie A. Carr,et al.  Imaging the Human Medial Temporal Lobe with High-Resolution fMRI , 2010, Neuron.

[19]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[20]  B. Bontempi,et al.  Time-dependent reorganization of brain circuitry underlying long-term memory storage , 1999, Nature.

[21]  Morris Moscovitch,et al.  A Hippocampal Marker of Recollection Memory Ability among Healthy Young Adults: Contributions of Posterior and Anterior Segments , 2011, Neuron.

[22]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[23]  Morris Moscovitch,et al.  Mechanisms of spontaneous confabulations: a strategic retrieval account. , 2006, Brain : a journal of neurology.

[24]  D. Hassabis,et al.  Decoding Individual Episodic Memory Traces in the Human Hippocampus , 2010, Current Biology.

[25]  I. L. Nieuwenhuis,et al.  The role of the ventromedial prefrontal cortex in memory consolidation , 2011, Behavioural Brain Research.

[26]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[27]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[28]  G. Winocur,et al.  Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. , 2004, Cerebral cortex.

[29]  Edith Lesburguères,et al.  Early Tagging of Cortical Networks Is Required for the Formation of Enduring Associative Memory , 2011, Science.

[30]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[31]  D. Hassabis,et al.  Patients with hippocampal amnesia cannot imagine new experiences , 2007, Proceedings of the National Academy of Sciences.

[32]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

[33]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[34]  R. Todd Constable,et al.  Evidence That Autobiographic Memory Retrieval Does Not Become Independent of the Hippocampus: An fMRI Study Contrasting Very Recent with Remote Events , 2005, Journal of Cognitive Neuroscience.

[35]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[36]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[37]  Nikolaus Weiskopf,et al.  Decoding Representations of Scenes in the Medial Temporal Lobes , 2011, Hippocampus.

[38]  Morris Moscovitch,et al.  As time goes by: Hippocampal connectivity changes with remoteness of autobiographical memory retrieval , 2012, Hippocampus.

[39]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[40]  M. Corballis,et al.  A role for the hippocampus in encoding simulations of future events , 2011, Proceedings of the National Academy of Sciences.

[41]  M Moscovitch,et al.  Hippocampal complex and retrieval of recent and very remote autobiographical memories: Evidence from functional magnetic resonance imaging in neurologically intact people , 2001, Hippocampus.

[42]  David G. Stork,et al.  Pattern Classification , 1973 .

[43]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Demis Hassabis,et al.  Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI , 2011, Learning & memory.

[45]  D. Hassabis,et al.  Scene Construction in Amnesia: An fMRI Study , 2012, The Journal of Neuroscience.

[46]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[47]  Tom den Heijer,et al.  Hippocampal Head Size Associated with Verbal Memory Performance in Nondemented Elderly , 2002, NeuroImage.

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

[49]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[51]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[52]  Y. Dudai The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[53]  K. Deisseroth,et al.  Dynamics of Retrieval Strategies for Remote Memories , 2011, Cell.

[54]  Eleanor A Maguire,et al.  Lateral Asymmetry in the Hippocampal Response to the Remoteness of Autobiographical Memories , 2003, The Journal of Neuroscience.

[55]  Demis Hassabis,et al.  Cortical midline involvement in autobiographical memory , 2009, NeuroImage.

[56]  Eric Halgren,et al.  Ecphory of autobiographical memories: An fMRI study of recent and remote memory retrieval , 2006, NeuroImage.

[57]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[58]  Jean-Claude Baron,et al.  Re-experiencing old memories via hippocampus: a PET study of autobiographical memory , 2004, NeuroImage.

[59]  Yasushi Miyashita,et al.  Behavioral/systems/cognitive Functional Dissociation between Anterior and Posterior Temporal Cortical Regions during Retrieval of Remote Memory , 2022 .

[60]  R. Deichmann,et al.  Real-time functional magnetic resonance imaging: methods and applications. , 2007, Magnetic resonance imaging.

[61]  Kazuhisa Niki,et al.  An fMRI Study on the Time-Limited Role of the Medial Temporal Lobe in Long-Term Topographical Autobiographic Memory , 2002, Journal of Cognitive Neuroscience.

[62]  G. Winocur,et al.  Memory Transformation and Systems Consolidation , 2011, Journal of the International Neuropsychological Society.

[63]  A. Gade,et al.  Temporal gradient in the remote memory impairment of amnesic patients with lesions in the basal forebrain , 1990, Neuropsychologia.

[64]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[65]  A. Wagner,et al.  Sources of Method Bias in Social Science Research and Recommendations on How to Control It , 2015 .

[66]  Yoram Singer,et al.  Reducing Multiclass to Binary: A Unifying Approach for Margin Classifiers , 2000, J. Mach. Learn. Res..

[67]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[68]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[69]  Thomas G. Dietterich,et al.  Solving Multiclass Learning Problems via Error-Correcting Output Codes , 1994, J. Artif. Intell. Res..

[70]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[71]  Isabelle Guyon,et al.  An Introduction to Variable and Feature Selection , 2003, J. Mach. Learn. Res..

[72]  Pascale Piolino,et al.  Hippocampal activation for autobiographical memories over the entire lifetime in healthy aged subjects: an fMRI study. , 2007, Cerebral cortex.

[73]  T. Teyler,et al.  The role of hippocampus in memory: A hypothesis , 1985, Neuroscience & Biobehavioral Reviews.

[74]  L. Nadel,et al.  Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time , 2007, Neural plasticity.

[75]  A. Hupbach,et al.  Memory formation, consolidation and transformation , 2012, Neuroscience & Biobehavioral Reviews.

[76]  D. Hassabis,et al.  Decoding Neuronal Ensembles in the Human Hippocampus , 2009, Current Biology.

[77]  M. Kopelman,et al.  Confabulation Extending across Episodic, Personal, and General Semantic Memory , 1997 .

[78]  R N Henson,et al.  Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories , 2001, Neuroreport.

[79]  U. Frith,et al.  The impact of extensive medial frontal lobe damage on 'Theory of Mind' and cognition. , 2004, Brain : a journal of neurology.

[80]  Mieke Verfaellie,et al.  Medial Temporal Lobe Damage Causes Deficits in Episodic Memory and Episodic Future Thinking Not Attributable to Deficits in Narrative Construction , 2011, The Journal of Neuroscience.

[81]  Armin Schnider,et al.  Spontaneous confabulators fail to suppress currently irrelevant memory traces , 1999, Nature Neuroscience.

[82]  Eleanor A. Maguire,et al.  Decoding information in the human hippocampus: A user's guide , 2012, Neuropsychologia.

[83]  Richard W. Hamming,et al.  Error detecting and error correcting codes , 1950 .