New learning following reactivation in the human brain: Targeting emotional memories through rapid serial visual presentation

Once reactivated, previously consolidated memories destabilize and have to be reconsolidated to persist, a process that might be altered non-invasively by interfering learning immediately after reactivation. Here, we investigated the influence of interference on brain correlates of reactivated episodic memories for emotional and neutral scenes using event-related potentials (ERPs). To selectively target emotional memories we applied a new reactivation method: rapid serial visual presentation (RSVP). RSVP leads to enhanced implicit processing (pop out) of the most salient memories making them vulnerable to disruption. In line, interference after reactivation of previously encoded pictures disrupted recollection particularly for emotional events. Furthermore, memory impairments were reflected in a reduced centro-parietal ERP old/new difference during retrieval of emotional pictures. These results provide neural evidence that emotional episodic memories in humans can be selectively altered through behavioral interference after reactivation, a finding with further clinical implications for the treatment of anxiety disorders.

[1]  L. Schwabe,et al.  Reactivation, interference, and reconsolidation: are recent and remote memories likewise susceptible? , 2011, Behavioral neuroscience.

[2]  L. Schwabe,et al.  Changing memories after reactivation: A one-time opportunity? , 2013, Neurobiology of Learning and Memory.

[3]  J. D. McGaugh.  Memory--a century of consolidation. , 2000, Science.

[4]  R. Dolan,et al.  Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Jens C. Pruessner,et al.  Neural Signature of Reconsolidation Impairments by Propranolol in Humans , 2012, Biological Psychiatry.

[6]  Georg Engel,et al.  Propranolol selectively blocks the enhanced parietal old/new effect during long-term recollection of unpleasant pictures: A high density ERP study , 2010, NeuroImage.

[7]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[8]  Joseph E LeDoux,et al.  Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats—a possible mechanism for the persistence of traumatic memories in PTSD , 2011, Depression and anxiety.

[9]  Jens C. Pruessner,et al.  Reconsolidation of Human Memory: Brain Mechanisms and Clinical Relevance , 2014, Biological Psychiatry.

[10]  M. Junghöfer,et al.  The selective processing of briefly presented affective pictures: an ERP analysis. , 2004, Psychophysiology.

[11]  M. Kindt,et al.  Beyond extinction: erasing human fear responses and preventing the return of fear , 2009, Nature Neuroscience.

[12]  K. Ressler,et al.  Implications of memory modulation for post-traumatic stress and fear disorders , 2013, Nature Neuroscience.

[13]  Joseph E LeDoux,et al.  Preventing the return of fear in humans using reconsolidation update mechanisms , 2010, Nature.

[14]  Ken A. Paller,et al.  Neural Substrates of Remembering – Electroencephalographic Studies , 2008 .

[15]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[16]  Michael R. Dulas,et al.  The effects of aging on emotion-induced modulations of source retrieval ERPs: Evidence for valence biases , 2012, Neuropsychologia.

[17]  A. Hupbach,et al.  Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. , 2007, Learning & memory.

[18]  J. K. Chan,et al.  Impairing existing declarative memory in humans by disrupting reconsolidation , 2013, Proceedings of the National Academy of Sciences.

[19]  Mary C. Potter,et al.  Recognition and Memory for Briefly Presented Scenes , 2012, Front. Psychology.

[20]  Rachel A Robbins,et al.  A Review and Clarification of the Terms “holistic,” “configural,” and “relational” in the Face Perception Literature , 2012, Front. Psychology.

[21]  E. Rolls.  The parietal cortex , 2001 .

[22]  A. Hamm,et al.  Enhanced long-term recollection for emotional pictures: evidence from high-density ERPs. , 2009, Psychophysiology.

[23]  Michael D. Rugg,et al.  Dissociation of the neural correlates of implicit and explicit memory , 1998, Nature.

[24]  Francesco Versace,et al.  Memory and event-related potentials for rapidly presented emotional pictures , 2010, Experimental Brain Research.

[25]  A. Hamm,et al.  Electrophysiological Signature of Emotional Memories , 2013 .

[26]  M Mishkin,et al.  Brain activity evidence for recognition without recollection after early hippocampal damage , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Markus Junghöfer,et al.  ElectroMagnetoEncephalography Software: Overview and Integration with Other EEG/MEG Toolboxes , 2011, Comput. Intell. Neurosci..

[28]  D Friedman,et al.  Event‐related potential (ERP) studies of memory encoding and retrieval: A selective review , 2000, Microscopy research and technique.

[29]  T. Agren,et al.  Human reconsolidation: A reactivation and update , 2014, Brain Research Bulletin.

[30]  Vera Ferrari,et al.  Repetition and brain potentials when recognizing natural scenes: task and emotion differences. , 2013, Social cognitive and affective neuroscience.

[31]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[32]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[33]  A. Yonelinas.  The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[34]  L. Schwabe,et al.  Updating of episodic memories depends on the strength of new learning after memory reactivation. , 2013, Behavioral neuroscience.

[35]  Kaia L. Vilberg,et al.  Functional significance of retrieval‐related activity in lateral parietal cortex: Evidence from fMRI and ERPs , 2009, Human brain mapping.

[36]  A. Hupbach,et al.  The dynamics of memory: context-dependent updating. , 2008, Learning & memory.

[37]  Marijn C. W. Kroes,et al.  β-Adrenergic Blockade during Memory Retrieval in Humans Evokes a Sustained Reduction of Declarative Emotional Memory Enhancement , 2010, The Journal of Neuroscience.

[38]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

[39]  P. Lang.  International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[40]  O. Hardt,et al.  A single standard for memory: the case for reconsolidation , 2009, Nature Reviews Neuroscience.

[41]  C. Forcato,et al.  The Role and Dynamic of Strengthening in the Reconsolidation Process in a Human Declarative Memory: What Decides the Fate of Recent and Older Memories? , 2013, PloS one.

[42]  A. Hamm,et al.  Emotional memories are resilient to time: Evidence from the parietal ERP old/new effect , 2011, Human brain mapping.

[43]  Lars Schwabe,et al.  Stress Sensitizes the Brain: Increased Processing of Unpleasant Pictures after Exposure to Acute Stress , 2012, Journal of Cognitive Neuroscience.

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

[45]  L. Cahill.  Why sex matters for neuroscience , 2006, Nature Reviews Neuroscience.

[46]  S. Luck.  An Introduction to the Event-Related Potential Technique , 2005 .

[47]  A. Frick,et al.  Disruption of Reconsolidation Erases a Fear Memory Trace in the Human Amygdala , 2012, Science.

[48]  K. Nader,et al.  Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval , 2000, Nature.