The effect of arousal on the emotional memory network depends on valence

Some suggest that arousal is the essential element needed to engage the amygdala. However, the role of arousal in the larger emotional memory network may differ depending on the valence (positive, negative) of the to-be-remembered information. The goal of the current study was to determine the influence of arousal-based changes in amygdalar connectivity for positive and negative items. Participants were shown emotional and neutral pictures while they underwent a functional magnetic resonance imaging (fMRI) scan. The emotional pictures varied by valence (positive or negative) and arousal (high or low). Approximately 90minutes later, outside of the scanner, participants took a surprise recognition test. Effective connectivity analysis examined how arousal affected successful encoding activity. For negative information, arousal increased the strength of amygdala connections to the inferior frontal gyrus and the middle occipital gyrus, while for positive information arousal decreased the strength of these amygdala efferents. Further, while the effect of arousal on memory for positive information was restricted to amygdalar efferents, arousal had a more widespread effect for negative items, enhancing connectivity between other nodes of the emotional memory network. These findings emphasize that the effect of arousal on the connectivity within the emotional memory network depends on item valence.

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

[2]  A P Shimamura,et al.  Source memory enhancement for emotional words. , 2001, Emotion.

[3]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[4]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[5]  Daniel Tranel,et al.  The influence of autonomic arousal and semantic relatedness on memory for emotional words. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[7]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Elizabeth A. Kensinger,et al.  Memory enhancement for emotional words: Are emotional words more vividly remembered than neutral words? , 2003, Memory & cognition.

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

[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]  Cheuk Y. Tang,et al.  Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: an fMRI study , 2001, Neuropsychologia.

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

[13]  R. Dolan,et al.  Amygdala Automaticity in Emotional Processing , 2003, Annals of the New York Academy of Sciences.

[14]  Katherine R. Mickley Steinmetz,et al.  The effects of valence and arousal on the neural activity leading to subsequent memory. , 2009, Psychophysiology.

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

[16]  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.

[17]  Ralph Adolphs,et al.  Processing of the Arousal of Subliminal and Supraliminal Emotional Stimuli by the Human Amygdala , 2003, The Journal of Neuroscience.

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

[19]  J. D. McGaugh,et al.  A Novel Demonstration of Enhanced Memory Associated with Emotional Arousal , 1995, Consciousness and Cognition.

[20]  A M Dale,et al.  Prefrontal‐hippocampal‐fusiform activity during encoding predicts intraindividual differences in free recall ability: An event‐related functional‐anatomic MRI study , 2007, Hippocampus.

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

[22]  John D E Gabrieli,et al.  Emotion enhances remembrance of neutral events past , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[23]  E. Kensinger,et al.  Remembering Emotional Experiences: The Contribution of Valence and Arousal , 2004, Reviews in the neurosciences.

[24]  Daniel L Schacter,et al.  When the Red Sox shocked the Yankees: Comparing negative and positive memories , 2006, Psychonomic bulletin & review.

[25]  E. Kensinger,et al.  Emotional valence influences the neural correlates associated with remembering and knowing , 2008, Cognitive, affective & behavioral neuroscience.

[26]  Michela Gamberini,et al.  Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas , 2006, The Journal of comparative neurology.

[27]  E. Stern,et al.  Linguistic threat activates the human amygdala. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  H. Klüver,et al.  "Psychic blindness" and other symptoms following bilateral temporal lobectomy in Rhesus monkeys. , 1937 .

[29]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[30]  J. Pardo,et al.  Elucidating Dynamic Brain Interactions with Across-Subjects Correlational Analyses of Positron Emission Tomographic Data: The Functional Connectivity of the Amygdala and Orbitofrontal Cortex during Olfactory Tasks , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  Daniel L. Schacter,et al.  Remembering the specific visual details of presented objects: Neuroimaging evidence for effects of emotion , 2007, Neuropsychologia.

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

[33]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[34]  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.

[35]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[36]  Larry Cahill,et al.  Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage , 2003, NeuroImage.

[37]  Daniel Tranel,et al.  Altered experience of emotion following bilateral amygdala damage , 2006, Cognitive neuropsychiatry.

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

[39]  John M Hoffman,et al.  Ecstasy and Agony: Activation of the Human Amygdala in Positive and Negative Emotion , 2002, Psychological science.

[40]  J. Gabrieli,et al.  Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience , 2000, The Journal of Neuroscience.

[41]  S. Hamann,et al.  Positive and negative emotional verbal stimuli elicit activity in the left amygdala , 2002, Neuroreport.

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

[43]  Larry Cahill,et al.  Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding , 2003, Neurobiology of Learning and Memory.

[44]  J. Russell,et al.  A Role for the Human Amygdala in Recognizing Emotional Arousal From Unpleasant Stimuli , 1999 .

[45]  S. Dewhurst,et al.  Emotionality, distinctiveness, and recollective experience , 2000 .

[46]  D. Amaral,et al.  Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey , 2003, Neuroscience.

[47]  G. V. Van Hoesen,et al.  Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. , 1977, Science.

[48]  Marcia K. Johnson,et al.  Phenomenal characteristics of memories for perceived and imagined autobiographical events. , 1988, Journal of experimental psychology. General.

[49]  Karl G. Jöreskog,et al.  Lisrel 8: Structural Equation Modeling With the Simplis Command Language , 1993 .

[50]  E. Kensinger Remembering the Details: Effects of Emotion , 2009, Emotion review : journal of the International Society for Research on Emotion.

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

[52]  Hanna Damasio,et al.  Amygdala contribution to selective dimensions of emotion. , 2007, Social cognitive and affective neuroscience.

[53]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

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

[55]  R. Dolan,et al.  Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures , 1999, Neuropsychologia.

[56]  Danielle S. Bassett,et al.  A validated network of effective amygdala connectivity , 2007, NeuroImage.

[57]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[58]  Thomas J. Ross,et al.  Amygdala response to both positively and negatively valenced stimuli , 2001, Neuroreport.

[59]  L. Weiskrantz,et al.  Behavioral changes associated with ablation of the amygdaloid complex in monkeys. , 1956, Journal of comparative and physiological psychology.