Same as it ever was: Vividness modulates the similarities and differences between the neural networks that support retrieving remote and recent autobiographical memories

The comparison of recent and remote autobiographical memories is often confounded by qualitative disparities across memories of different ages, such as vividness. In this study, ten individuals prospectively collected audio recordings that were used to cue memories of recent (~1 month old) and remote (~1.5 year old) everyday events. Because the retrieval cues were recorded at the time of event, they were highly potent. Although remote events did not differ in novelty, importance, or emotional change at the time at the time of encoding, half of the cues for these events induced retrieval comparable in vividness to recent events (all of which were vividly re-experienced). Recent and remote vivid memories were associated with a neural pattern that included right frontal, left parietal and limbic regions that were active early in the retrieval period. Non-vivid remote memories were associated with a later onset of a bilateral distributed pattern that included regions in the frontal, parietal, and temporal lobes. Functional connectivity analysis indicated that the left anterior hippocampus was co-activated with bilateral frontal, parahippocampal, and parietal regions for vivid memories (irrespective of memory age) early in the retrieval period, whereas non-vivid memories, alongside recent memories, showed later and broader co-activation with frontal, parietal, occipital, and temporal regions. The absence of a significant difference between the recent and remote vivid memories may be due to insufficient power to detect potential subtle differences between these conditions. Nonetheless, there was evidence for different patterns of hippocampal-neocortical connectivity for remote memories and recent memories, irrespective of vividness. These findings suggest that while there is a functional shift in hippocampal connectivity that is associated with memory age when very recent events are used, vividness is strongly associated with both activation and functional connectivity patterns irrespective of memory age.

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

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

[3]  L. Squire,et al.  The Fate of Old Memories after Medial Temporal Lobe Damage , 2006, The Journal of Neuroscience.

[4]  Ramona O. Hopkins,et al.  The Neuroanatomy of Remote Memory , 2005, Neuron.

[5]  Donna Rose Addis,et al.  The neural correlates of specific versus general autobiographical memory construction and elaboration , 2011, Neuropsychologia.

[6]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[7]  Brian Levine,et al.  The Functional Neuroanatomy of Episodic and Semantic Autobiographical Remembering: A Prospective Functional MRI Study , 2004, Journal of Cognitive Neuroscience.

[8]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[9]  Donald T. Stuss,et al.  Common and Unique Neural Correlates of Autobiographical Memory and Theory of Mind , 2010, Journal of Cognitive Neuroscience.

[10]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[11]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[12]  D C Rubin,et al.  The distribution of autobiographical memories across the lifespan , 1997, Memory & cognition.

[13]  Asaf Gilboa,et al.  Autobiographical and episodic memory—one and the same? Evidence from prefrontal activation in neuroimaging studies , 2004, Neuropsychologia.

[14]  D. Rubin,et al.  The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving. , 2008, Cerebral cortex.

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

[16]  L. Nadel,et al.  Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results , 2000, Hippocampus.

[17]  R. Sutherland,et al.  Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories , 2007, The European journal of neuroscience.

[18]  M Baulac,et al.  Autobiographical memory after temporal lobe resection: neuropsychological and MRI volumetric findings. , 2007, Brain : a journal of neurology.

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

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

[21]  Yiping P Du,et al.  Reducing susceptibility artifacts in fMRI using volume‐selective z‐shim compensation , 2007, Magnetic resonance in medicine.

[22]  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.

[23]  Kevin S. LaBar,et al.  Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval , 2005, Neuropsychologia.

[24]  D. Addis,et al.  Differential neural activity during search of specific and general autobiographical memories elicited by musical cues , 2011, Neuropsychologia.

[25]  Daniel L. Schacter,et al.  Routes to the past: Neural substrates of direct and generative autobiographical memory retrieval , 2012, NeuroImage.

[26]  Natasa Kovacevic,et al.  Patterns of Autobiographical Memory Loss in Medial-Temporal Lobe Amnesic Patients , 2008, Journal of Cognitive Neuroscience.

[27]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[28]  C. Brock Kirwan,et al.  Detailed recollection of remote autobiographical memory after damage to the medial temporal lobe , 2008, Proceedings of the National Academy of Sciences.

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

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

[31]  R. Constable,et al.  Composite image formation in z‐shimmed functional MR imaging , 1999, Magnetic resonance in medicine.

[32]  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.

[33]  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.

[34]  E. Tulving [Episodic memory: from mind to brain]. , 2004, Revue neurologique.

[35]  Brian Levine,et al.  Theta oscillations orchestrate medial temporal lobe and neocortex in remembering autobiographical memories , 2014, NeuroImage.

[36]  M. Fanselow,et al.  Temporally Graded Retrograde Amnesia of Contextual Fear after Hippocampal Damage in Rats: Within-Subjects Examination , 1999, The Journal of Neuroscience.

[37]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[38]  E A Maguire,et al.  Neuroimaging, memory and the human hippocampus. , 2001, Revue neurologique.

[39]  Morris Moscovitch,et al.  Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial memory , 2005, Neuropsychologia.

[40]  E. Schuman,et al.  Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory , 2004, Nature.

[41]  David C. Rubin,et al.  The Neuropsychology of Autobiographical Memory , 2003, Cortex.

[42]  B. Levine,et al.  Behavioral and functional neuroanatomical correlates of anterograde autobiographical memory in isolated retrograde amnesic patient M.L. , 2009, Neuropsychologia.

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

[44]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[45]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[46]  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.

[47]  Donna Rose Addis,et al.  Amygdala activity at encoding corresponds with memory vividness and with memory for select episodic details , 2011, Neuropsychologia.

[48]  Ramona O Hopkins,et al.  Successful Recollection of Remote Autobiographical Memories by Amnesic Patients with Medial Temporal Lobe Lesions , 2003, Neuron.

[49]  L R Squire,et al.  Amnesia, memory and brain systems. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[51]  C. Thompson Autobiographical Memory : Theoretical and Applied Perspectives , 2014 .

[52]  M. Conway Sensory-perceptual episodic memory and its context: autobiographical memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[55]  M. Conway,et al.  Organization in autobiographical memory , 1987, Memory & cognition.

[56]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[57]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[58]  R. Cabeza,et al.  Functional neuroimaging of autobiographical memory , 2007, Trends in Cognitive Sciences.

[59]  D. Rubin,et al.  Properties of Word Cues for Autobiographical Memory , 1997, Psychological reports.

[60]  S. Corkin,et al.  Medial temporal lobe structures are needed to re-experience remote autobiographical memories: evidence from H.M. and W.R. , 2005, Neuropsychologia.

[61]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

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

[63]  Morris Moscovitch,et al.  The hippocampus as a "stupid," domain-specific module: Implications for theories of recent and remote memory, and of imagination. , 2008, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.