Emotional valence influences the neural correlates associated with remembering and knowing

In the present study, we examined whether emotional valence modulates the neural processes that are engaged during the encoding of information that is later vividly remembered versus that which is only known to be familiar. Participants underwent an fMRI scan while viewing positive, negative, and neutral stimuli. Later, recognized items were labeled as either remembered or known. Negative items that were later vividly remembered recruited temporo-occipital regions associated with sensory processing more than did positive or neutral items that were vividly remembered. The encoding of positive information later known recruited the cingulate gyrus and bilateral frontal and parietal areas—regions associated with episodic and semantic retrieval and self-referential processing—more than did the encoding of negative or neutral items that were later known. These results suggest that memories for negative items may be vividly recollected due to increased sensory processing during encoding, whereas enhanced gist-based processing of positive information may lead to increased feelings of familiarity.

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

[2]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

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

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

[5]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[6]  Joseph R. Manns,et al.  Recognition Memory and the Human Hippocampus , 2003, Neuron.

[7]  D. Schacter,et al.  Memory and emotion , 2008 .

[8]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[9]  K. Ochsner,et al.  Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. , 2000, Journal of experimental psychology. General.

[10]  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.

[11]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[12]  J. D. McGaugh,et al.  Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[14]  W. Montague,et al.  Category norms of verbal items in 56 categories A replication and extension of the Connecticut category norms , 1969 .

[15]  Peter E. Wais,et al.  The Hippocampus Supports both the Recollection and the Familiarity Components of Recognition Memory , 2006, Neuron.

[16]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  E. Phelps,et al.  Arousal-Mediated Memory Consolidation: Role of the Medial Temporal Lobe in Humans , 1998 .

[18]  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.

[19]  Daniel L Schacter,et al.  Effects of emotion on memory specificity in young and older adults. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[20]  Daniel L. Schacter,et al.  Emotional content and reality-monitoring ability: fMRI evidence for the influences of encoding processes , 2005, Neuropsychologia.

[21]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[22]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[23]  T. Schormann,et al.  Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. , 2000, Brain : a journal of neurology.

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

[25]  L. Jacoby A process dissociation framework: Separating automatic from intentional uses of memory , 1991 .

[26]  Katherine A. Rawson,et al.  Category Norms: An Updated and Expanded Version of the Battig and Montague (1969) Norms. , 2004 .

[27]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[28]  Rachel J. Garoff-Eaton,et al.  Effects of Emotion on Memory Specificity: Memory Trade-Offs Elicited by Negative Visually Arousing Stimuli. , 2007 .

[29]  Andrew P Yonelinas,et al.  Dissociating familiarity from recollection using rote rehearsal , 2004, Memory & cognition.

[30]  Scott D. Slotnick,et al.  Support for a continuous (single-process) model of recognition memory and source memory , 2005, Memory & cognition.

[31]  R. Dolan,et al.  Encoding of emotional memories depends on amygdala and hippocampus and their interactions , 2004, Nature Neuroscience.

[32]  Daniel Tranel,et al.  Preferring one taste over another without recognizing either , 2005, Nature Neuroscience.

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

[34]  Karen Gasper Do you see what I see? Affect and visual information processing , 2004 .

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

[36]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[37]  Florin Dolcos,et al.  Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: an event-related fMRI study , 2004, NeuroImage.

[38]  A. Anderson Affective influences on the attentional dynamics supporting awareness. , 2005, Journal of experimental psychology. General.

[39]  L. Davachi,et al.  Hippocampal contributions to episodic encoding: insights from relational and item-based learning. , 2002, Journal of neurophysiology.

[40]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[41]  Karen Gasper,et al.  Attending to the Big Picture: Mood and Global Versus Local Processing of Visual Information , 2002, Psychological science.

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

[43]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

[44]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[45]  Michael Wilson MRC Psycholinguistic Database , 2001 .

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

[47]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

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

[49]  L R Squire,et al.  Remembering and knowing: two different expressions of declarative memory. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[50]  N. Schwarz,et al.  Mood and the impact of category membership and individuating information , 1996 .

[51]  M. Bradley,et al.  Affective Norms for English Words (ANEW): Instruction Manual and Affective Ratings , 1999 .

[52]  L. Pessoa,et al.  Positive emotions broaden the scope of attention and thought‐action repertoires , 2005, Cognition & emotion.

[53]  G. Mandler Recognizing: The judgment of previous occurrence. , 1980 .

[54]  A. Anderson,et al.  Positive affect increases the breadth of attentional selection , 2007, Proceedings of the National Academy of Sciences.

[55]  E. Glisky,et al.  Is flashbulb memory a special instance of source memory? Evidence from older adults , 2002, Memory.

[56]  Rachel J. Garoff-Eaton,et al.  Memory for Specific Visual Details can be Enhanced by Negative Arousing Content. , 2006 .

[57]  M. Bradley,et al.  Affective Normsfor English Words (ANEW): Stimuli, instruction manual and affective ratings (Tech Report C-1) , 1999 .

[58]  Daniel Tranel,et al.  Amygdala damage impairs emotional memory for gist but not details of complex stimuli , 2005, Nature Neuroscience.

[59]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Seth J. Ramus,et al.  Linking affect to action: critical contributions of the orbitofrontal cortex. Preface. , 2007, Annals of the New York Academy of Sciences.

[61]  M. Petrides The Orbitofrontal Cortex: Novelty, Deviation from Expectation, and Memory , 2007, Annals of the New York Academy of Sciences.

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

[63]  Tali Sharot,et al.  How emotion enhances the feeling of remembering , 2004, Nature Neuroscience.