fMRI correlates of the episodic retrieval of emotional contexts

Functional neuroimaging studies reveal differences in neural correlates of the retrieval of emotional and nonemotional memories. In the present experiment, encoding of emotionally neutral pictures in association with positively, neutrally or negatively valenced background contexts led to differential modulation of neural activity elicited in a subsequent recognition memory test for these pictures. Recognition of stimuli previously studied in emotional compared to neutral contexts elicited enhanced activity in structures previously implicated in episodic memory, including the parahippocampal cortex, hippocampus and prefrontal cortex. In addition, there was engagement of structures linked more specifically to emotional processing, including the amygdala, orbitofrontal cortex and anterior cingulate cortex. These emotion-related effects displayed both valence-independent and valence-specific components. We discuss the findings in terms of current models of emotional memory retrieval.

[1]  J. Desmond,et al.  Neural Substrates of Fluid Reasoning: An fMRI Study of Neocortical Activation during Performance of the Raven's Progressive Matrices Test , 1997, Cognitive Psychology.

[2]  R. Henson,et al.  A familiarity signal in human anterior medial temporal cortex? , 2003, Hippocampus.

[3]  Hugo D. Critchley,et al.  Volitional Control of Autonomic Arousal: A Functional Magnetic Resonance Study , 2002, NeuroImage.

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

[5]  Karl J. Friston,et al.  Amygdala–Hippocampal Involvement in Human Aversive Trace Conditioning Revealed through Event-Related Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[6]  Arthur P. Wunderlich,et al.  Emotional context modulates subsequent memory effect , 2003, NeuroImage.

[7]  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.

[8]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[9]  Andrzej Urbanik,et al.  Central control of heart rate changes during visual affective processing as revealed by fMRI. , 2003, Acta neurobiologiae experimentalis.

[10]  Michael D. Rugg,et al.  Event-Related Potential Correlates of the Retrieval of Emotional and Nonemotional Context , 2004, Journal of Cognitive Neuroscience.

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

[12]  A. Young,et al.  Impaired recognition and experience of disgust following brain injury , 2000, Nature Neuroscience.

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

[14]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[15]  Daniel C. Krawczyk,et al.  Contributions of the prefrontal cortex to the neural basis of human decision making , 2002, Neuroscience & Biobehavioral Reviews.

[16]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Theory , 2002, NeuroImage.

[17]  F. Barkhof,et al.  Anterior Medial Temporal Lobe Activation during Attempted Retrieval of Encoded Visuospatial Scenes: An Event-Related fMRI Study , 2001, NeuroImage.

[18]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[19]  C. Price.  The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[20]  T. Shallice,et al.  Confidence in Recognition Memory for Words: Dissociating Right Prefrontal Roles in Episodic Retrieval , 2000, Journal of Cognitive Neuroscience.

[21]  R. Buckner,et al.  Neural Correlates of Episodic Retrieval Success , 2000, NeuroImage.

[22]  C. Stark,et al.  Making Memories without Trying: Medial Temporal Lobe Activity Associated with Incidental Memory Formation during Recognition , 2003, The Journal of Neuroscience.

[23]  S. G. Cox,et al.  Functional MRI study of the cognitive generation of affect. , 1999, The American journal of psychiatry.

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

[25]  H. Critchley,et al.  Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans , 2000, The Journal of physiology.

[26]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[27]  M. Gazzaniga,et al.  The new cognitive neurosciences , 2000 .

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

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

[30]  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.

[31]  Jonathan D. Cohen,et al.  Anterior Cingulate Cortex, Conflict Monitoring, and Levels of Processing , 2001, NeuroImage.

[32]  R. Dolan,et al.  Dissociable Temporal Lobe Activations during Emotional Episodic Memory Retrieval , 2000, NeuroImage.

[33]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[34]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.

[35]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[36]  R. Henson,et al.  The neural basis of episodic memory: evidence from functional neuroimaging. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[37]  M. Gazzaniga.  The new cognitive neurosciences, 2nd ed. , 2000 .

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

[39]  R. Cabeza,et al.  Neural bases of learning and memory: functional neuroimaging evidence , 2000, Current opinion in neurology.

[40]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[41]  J. D. McGaugh,et al.  Involvement of the amygdala in memory storage: interaction with other brain systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  Rugg,et al.  Memory retrieval: an electrophysiological perspective , 1999 .

[44]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

[45]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

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

[47]  Thomas E. Nichols,et al.  Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: a fMRI study , 2003, Biological Psychiatry.

[48]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[49]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[50]  L Cahill.  A neurobiological perspective on emotionally influenced, long-term memory. , 1999, Seminars in clinical neuropsychiatry.

[51]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[52]  R. Henson,et al.  State-related and item-related neural correlates of successful memory encoding , 2002, Nature Neuroscience.