Two routes to emotional memory: distinct neural processes for valence and arousal.

Prior investigations have demonstrated that emotional information is often better remembered than neutral information, but they have not directly contrasted effects attributable to valence and those attributable to arousal. By using functional MRI and behavioral studies, we found that distinct cognitive and neural processes contribute to emotional memory enhancement for arousing information versus valenced, nonarousing information. The former depended on an amygdalar-hippocampal network, whereas the latter was supported by a prefrontal cortex-hippocampal network implicated in controlled encoding processes. A behavioral companion study, with a divided-attention paradigm, confirmed that memory enhancement for valenced, nonarousing words relied on controlled encoding processes: concurrent task performance reduced the enhancement effect. Enhancement for arousing words occurred automatically, even when encoding resources were diverted to the secondary task.

[1]  H. Klüver,et al.  PRELIMINARY ANALYSIS OF FUNCTIONS OF THE TEMPORAL LOBES IN MONKEYS , 1939 .

[2]  Eliot Slater Psychobiology , 1949 .

[3]  J. Winn,et al.  Brain , 1878, The Lancet.

[4]  J. Russell A circumplex model of affect. , 1980 .

[5]  D. Amaral,et al.  An autoradiographic study of the projections of the central nucleus of the monkey amygdala , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  J. D. McGaugh,et al.  Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. , 1990, Behavioral neuroscience.

[7]  O. John,et al.  Automatic vigilance: the attention-grabbing power of negative social information. , 1991, Journal of personality and social psychology.

[8]  P. Eslinger The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction edited by J.P. Aggleton, Wiley-Liss, 1992. $125.00 (xii + 615 pages) ISBN 0 4715 6129 0 , 1992, Trends in Neurosciences.

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

[10]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[11]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[12]  A behavioral probe of the growth of intake potential during the inter-meal interval in the rat. , 1994, Behavioral neuroscience.

[13]  James L. McGaugh,et al.  The amygdala and emotional memory , 1995, Nature.

[14]  Joseph E LeDoux Emotion: clues from the brain. , 1995, Annual review of psychology.

[15]  T. Dalgleish,et al.  The emotional Stroop task and psychopathology. , 1996, Psychological bulletin.

[16]  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.

[17]  F. Craik,et al.  The effects of divided attention on encoding and retrieval processes in human memory. , 1996, Journal of experimental psychology. General.

[18]  Dennis D. Spencer,et al.  Memory for Emotional Words Following Unilateral Temporal Lobectomy , 1997, Brain and Cognition.

[19]  Rina Schul,et al.  Impaired declarative memory for emotional material following bilateral amygdala damage in humans. , 1997 .

[20]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[21]  A M Dale,et al.  Randomized event‐related experimental designs allow for extremely rapid presentation rates using functional MRI , 1998, Neuroreport.

[22]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

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

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

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

[26]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[28]  L. Cahill,et al.  The Role of Overt Rehearsal in Enhanced Conscious Memory for Emotional Events , 1999, Consciousness and Cognition.

[29]  T. Dalgleish,et al.  Handbook of cognition and emotion , 1999 .

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

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

[32]  Gary H. Glover,et al.  fMRI identifies a network of structures correlated with retention of positive and negative emotional memory , 1999, Psychobiology.

[33]  P. Benson,et al.  Towards a functional neuroanatomy of self processing: effects of faces and words. , 2000, Brain research. Cognitive brain research.

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

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

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

[37]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[38]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[39]  I. Tendolkar,et al.  Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level , 2001, Brain Research Bulletin.

[40]  Hannu J. Aronen,et al.  Working Memory of Identification of Emotional Vocal Expressions: An fMRI Study , 2001, NeuroImage.

[41]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[42]  Stephan Hamann,et al.  Cognitive and neural mechanisms of emotional memory , 2001, Trends in Cognitive Sciences.

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

[44]  Tom Manly,et al.  Coffee in the cornflakes: time-of-day as a modulator of executive response control , 2002, Neuropsychologia.

[45]  R. Cabeza,et al.  Event-related potentials of emotional memory: Encoding pleasant, unpleasant, and neutral pictures , 2002, Cognitive, affective & behavioral neuroscience.

[46]  R. Dolan,et al.  Emotion, Cognition, and Behavior , 2002, Science.

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

[48]  C. B. Puryear,et al.  The Contribution of the Amygdala to Conditioned Thalamic Arousal , 2002, The Journal of Neuroscience.

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

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

[51]  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.

[52]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. Oaksford,et al.  Emotional cognition: from brain to behaviour , 2002 .

[54]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[55]  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.

[56]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[57]  R. Dolan,et al.  An emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Larry Cahill,et al.  Sex- and hemisphere-related influences on the neurobiology of emotionally influenced memory , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.