Emotional context modulates subsequent memory effect

Emotions have been shown to modulate memory processes. However, the neuronal substrate underlying these modulatory effects is largely unknown. Using event-related functional magnetic resonance imaging (fMRI), we investigated whether the context of emotional encoding modulates brain activation predictive for subsequent recall of emotionally neutral material. While inferior frontal activation predicted recall in general, our data show that in a positive encoding context, recall was predicted by activation of right anterior parahippocampal and extrastriate visual brain areas, whereas in a negative encoding context, recall was predicted by activation of the amygdala. Thus, we could demonstrate that successful episodic encoding is differentially modulated by emotional context. These results contribute to the understanding of the interaction of emotion and cognition and moreover are of general relevance for studies of episodic memory.

[1]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[2]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  J. D. McGaugh,et al.  Beta-adrenergic activation and memory for emotional events. , 1994, Nature.

[4]  U. Habel,et al.  Gender differences in regional cerebral activity during sadness , 2000, Human brain mapping.

[5]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[6]  R. Maddock,et al.  Time course of the subjective emotional response to aversive pictures: relevance to fMRI studies , 2001, Psychiatry Research: Neuroimaging.

[7]  R. Adolphs,et al.  Impaired declarative memory for emotional material following bilateral amygdala damage in humans. , 1997, Learning & memory.

[8]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[9]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[10]  J. Borod,et al.  Interhemispheric and intrahemispheric control of emotion: a focus on unilateral brain damage. , 1992, Journal of consulting and clinical psychology.

[11]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[12]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[14]  Joseph P. Forgas,et al.  Emotion and Social Judgments , 2020 .

[15]  Klaus Fiedler,et al.  On the Task, the Measures and the Mood in Research on Affect and Social Cognition , 1991 .

[16]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[17]  Michael D. Rugg,et al.  Electrophysiological Correlates of the Retrieval of Emotional and Non-emotional Context , 2001, Journal of Cognitive Neuroscience.

[18]  E. Gordon,et al.  Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording , 2001, NeuroImage.

[19]  A. Damasio Descartes’ Error. Emotion, Reason and the Human Brain. New York (Grosset/Putnam) 1994. , 1994 .

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

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

[22]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[23]  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.

[24]  Joseph P Newman,et al.  Deficient response modulation and emotion processing in low-anxious Caucasian psychopathic offenders: results from a lexical decision task. , 2002, Emotion.

[25]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[26]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[27]  K Lehnertz,et al.  Real-time tracking of memory formation in the human rhinal cortex and hippocampus. , 1999, Science.

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

[29]  D. Levine,et al.  A neuropsychological theory of positive affect and its influence on cognition. , 1999, Psychological review.

[30]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[31]  L. Heimer,et al.  Substantia innominata: a notion which impedes clinical–anatomical correlations in neuropsychiatric disorders , 1997, Neuroscience.

[32]  R. J. Dolan,et al.  Parallel Neural Responses in Amygdala Subregions and Sensory Cortex during Implicit Fear Conditioning , 2001, NeuroImage.

[33]  O Josephs,et al.  Dissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding , 2002, The Journal of Neuroscience.

[34]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[35]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[36]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Nick Medford,et al.  Effects of normal aging and Alzheimer's disease on emotional memory. , 2002, Emotion.

[38]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[39]  R. Dolan,et al.  Neural Activation during Covert Processing of Positive Emotional Facial Expressions , 1996, NeuroImage.

[40]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[41]  Steven G. Potkin,et al.  Sex-Related Difference in Amygdala Activity during Emotionally Influenced Memory Storage , 2001, Neurobiology of Learning and Memory.

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

[43]  R. Henson,et al.  Neural activity associated with episodic memory for emotional context , 2001, Neuropsychologia.

[44]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[45]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.