The role of medial temporal lobe in item recognition and source recollection of emotional stimuli

Recent neuroimaging results suggest that distinct regions within the medial temporal lobe (MTL) may differentially support the episodic encoding of item and relational information for nonemotional stimuli (for a review, see Davachi, 2006). The present study was designed to assess whether these findings generalize to emotional stimuli. Behaviorally, we found that emotion reduced item recognition accuracy but did not reliably affect relational memory. fMRI analyses revealed that neutral and emotional words elicited distinct activation patterns within MTL regions predictive of subsequent memory. Consistent with previous findings for neutral words, hippocampal activation predicted later relational memory, whereas activation in the perirhinal cortex predicted successful item recognition. However, for emotional words, activation in the amygdala, hippocampus, and posterior parahippocampal cortex predicted item recognition only. These data suggest that MTL regions differentially support encoding of neutral and emotional stimuli.

[1]  I. Saul,et al.  Ischemic Preconditioning Targets the Respiration of Synaptic Mitochondria via Protein Kinase Cε , 2008, The Journal of Neuroscience.

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

[3]  Daniel Reisberg,et al.  Remembering emotional events , 1992, Memory & cognition.

[4]  D. Amaral,et al.  Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys , 1996, The Journal of comparative neurology.

[5]  Russell A. Epstein,et al.  Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex , 2001, Cognitive neuropsychology.

[6]  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.

[7]  R. Burchfield.  Frequency Analysis of English Usage: Lexicon and Grammar. By W. Nelson Francis and Henry Kučera with the assistance of Andrew W. Mackie. Boston: Houghton Mifflin. 1982. x + 561 , 1985 .

[8]  L. Davachi,et al.  Behavioral/systems/cognitive Functional–neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory , 2022 .

[9]  Lila Davachi,et al.  Behavioral / Systems / Cognitive Differential Encoding Mechanisms for Subsequent Associative Recognition and Free Recall , 2012 .

[10]  C. Stark,et al.  Medial temporal lobe activation during encoding and retrieval of novel face-name pairs , 2004, Hippocampus.

[11]  Ramona O Hopkins,et al.  Item memory, source memory, and the medial temporal lobe: concordant findings from fMRI and memory-impaired patients. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[13]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[14]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

[15]  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.

[16]  Michael D Rugg,et al.  Encoding and the Durability of Episodic Memory: A Functional Magnetic Resonance Imaging Study , 2005, The Journal of Neuroscience.

[17]  Daniel L Schacter,et al.  Encoding activity in anterior medial temporal lobe supports subsequent associative recognition , 2004, NeuroImage.

[18]  D Tsivilis,et al.  Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition , 2004, Hippocampus.

[19]  Marta Kutas,et al.  Electrophysiological Correlates of Emotion-Induced Recognition Bias , 2001, Journal of Cognitive Neuroscience.

[20]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

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

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

[23]  W. Nelson Francis,et al.  FREQUENCY ANALYSIS OF ENGLISH USAGE: LEXICON AND GRAMMAR , 1983 .

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

[25]  Mara Mather,et al.  Emotional Arousal Can Impair Feature Binding in Working Memory , 2006, Journal of Cognitive Neuroscience.

[26]  B R Rosen,et al.  Encoding novel face‐name associations: A functional MRI study , 2001, Human brain mapping.

[27]  R. Marsh,et al.  Source monitoring is not always enhanced for valenced material , 2007, Memory & cognition.

[28]  L. Mannucci,et al.  Chemical Stimulation of Synaptosomes Modulates α-Ca2+/Calmodulin-Dependent Protein Kinase II mRNA Association to Polysomes , 2000, The Journal of Neuroscience.

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

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

[31]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Robert T. Knight,et al.  Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity , 2002, Nature Neuroscience.

[33]  Andrew P. Yonelinas,et al.  Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology , 2005, Neuropsychologia.

[34]  Anthony D Wagner,et al.  Memory orientation and success: separable neurocognitive components underlying episodic recognition , 2003, Neuropsychologia.

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

[36]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. Phelps.  Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

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

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

[40]  L. Davachi.  Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[41]  Ken A Paller,et al.  Neural Evidence That Vivid Imagining Can Lead to False Remembering , 2004, Psychological science.

[42]  Peter W. Foltz,et al.  An introduction to latent semantic analysis , 1998 .

[43]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[44]  Adam K. Anderson,et al.  Specifying the Contributions of the Human Amygdala to Emotional Memory : A Case Study , 2008 .

[45]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[46]  N. Hunkin,et al.  Relative sparing of item recognition memory in a patient with adult‐onset damage limited to the hippocampus , 2002, Hippocampus.

[47]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[48]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

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

[50]  Tali Sharot,et al.  How personal experience modulates the neural circuitry of memories of September 11 , 2007, Proceedings of the National Academy of Sciences.

[51]  Brian Knutson,et al.  Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation , 2006, Neuron.

[52]  C. Richard Puff,et al.  Memory Organization and Structure , 1979 .

[53]  J. Easterbrook.  The effect of emotion on cue utilization and the organization of behavior. , 1959, Psychological review.

[54]  Arnaud D'Argembeau,et al.  Influence of affective meaning on memory for contextual information. , 2004, Emotion.

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

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

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