Dynamic Modulation of Amygdala–Hippocampal Connectivity by Emotional Arousal

Positive and negative emotional events are better remembered than neutral events. Studies in animals suggest that this phenomenon depends on the influence of the amygdala upon the hippocampus. In humans, however, it is largely unknown how these two brain structures functionally interact and whether these interactions are similar between positive and negative information. Using dynamic causal modeling of fMRI data in 586 healthy subjects, we show that the strength of the connection from the amygdala to the hippocampus was rapidly and robustly increased during the encoding of both positive and negative pictures in relation to neutral pictures. We also observed an increase in connection strength from the hippocampus to the amygdala, albeit at a smaller scale. These findings indicate that, during encoding, emotionally arousing information leads to a robust increase in effective connectivity from the amygdala to the hippocampus, regardless of its valence.

[1]  R. Doty.  Memory and Emotion: The Making of Lasting Memories.Maps of the Mind.ByJames L McGaugh.New York: Columbia University Press. $24.50. xi + 162 p; ill.; index. ISBN: 0–231–12022–2. 2003. , 2004 .

[2]  Xiaoping Hu,et al.  Investigating Effective Brain Connectivity from fMRI Data: Past Findings and Current Issues with Reference to Granger Causality Analysis , 2012, Brain Connect..

[3]  Rainer Goebel,et al.  The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution , 2011, NeuroImage.

[4]  D. Schacter,et al.  Processing emotional pictures and words: Effects of valence and arousal , 2006, Cognitive, affective & behavioral neuroscience.

[5]  Karl J. Friston,et al.  Model selection and gobbledygook: Response to Lohmann et al. , 2013, NeuroImage.

[6]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[7]  J. D. McGaugh.  Memory consolidation and the amygdala: a systems perspective , 2002, Trends in Neurosciences.

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

[9]  J. D. McGaugh,et al.  Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions , 2010, Neurobiology of Learning and Memory.

[10]  J. D. McGaugh,et al.  Basolateral Amygdala Lesions Block the Memory‐enhancing Effect of Glucocorticoid Administration in the Dorsal Hippocampus of Rats , 1997, The European journal of neuroscience.

[11]  Karl J. Friston,et al.  Recognizing Sequences of Sequences , 2009, PLoS Comput. Biol..

[12]  J. Voogd,et al.  The Human Central Nervous System , 1978, Springer Berlin Heidelberg.

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

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

[15]  J. D. McGaugh,et al.  Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[16]  K. Luan Phan,et al.  The contextual brain: implications for fear conditioning, extinction and psychopathology , 2013, Nature Reviews Neuroscience.

[17]  Donna Rose Addis,et al.  The effect of arousal on the emotional memory network depends on valence , 2010, NeuroImage.

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

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

[20]  M. Seghier,et al.  Reading Aloud Boosts Connectivity through the Putamen , 2009, Cerebral cortex.

[21]  D L Rosene,et al.  Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: II. Reciprocal and non‐reciprocal connections , 1988, The Journal of comparative neurology.

[22]  R. Cabeza,et al.  Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. , 2008, Cerebral cortex.

[23]  R. Heimberg,et al.  Memory biases in the anxiety disorders: current status. , 2002, Clinical psychology review.

[24]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[25]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[26]  Mark D'Esposito,et al.  The continuing challenge of understanding and modeling hemodynamic variation in fMRI , 2012, NeuroImage.

[27]  Klaas E. Stephan,et al.  Dynamic causal modelling: A critical review of the biophysical and statistical foundations , 2011, NeuroImage.

[28]  Karl J. Friston,et al.  Modelling functional integration: a comparison of structural equation and dynamic causal models , 2004, NeuroImage.

[29]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[30]  T. Teyler.  Long-term potentiation and memory. , 1987, International journal of neurology.

[31]  Michael S C Thomas,et al.  Multiple Routes from Occipital to Temporal Cortices during Reading , 2011, The Journal of Neuroscience.

[32]  A. Anderson,et al.  Shared Neural Substrates of Emotionally Enhanced Perceptual and Mnemonic Vividness , 2013, Front. Behav. Neurosci..

[33]  Gal Richter-Levin,et al.  Emotional tagging—A simple hypothesis in a complex reality , 2011, Progress in Neurobiology.

[34]  Marte Swart,et al.  Variation of the gene coding for DARPP-32 (PPP1R1B) and brain connectivity during associative emotional learning , 2012, NeuroImage.

[35]  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.

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

[37]  R. Dolan,et al.  Task and Content Modulate Amygdala-Hippocampal Connectivity in Emotional Retrieval , 2006, Neuron.

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

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

[40]  H. Pashler,et al.  Enhanced memory for negatively emotionally charged pictures without selective rumination. , 2005, Emotion.

[41]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[42]  A. Etkin,et al.  Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. , 2007, The American journal of psychiatry.

[43]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[44]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[45]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[46]  J L McGaugh,et al.  Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[47]  H. Critchley,et al.  Neural correlates of processing valence and arousal in affective words. , 2006, Cerebral cortex.

[48]  Karl J. Friston,et al.  Dynamic causal modelling for fMRI: A two-state model , 2008, NeuroImage.

[49]  P. Lang.  International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

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

[51]  E. Kensinger,et al.  What Factors Need to be Considered to Understand Emotional Memories? , 2009, Emotion review : journal of the International Society for Research on Emotion.

[52]  Thomas Elbert,et al.  A deletion variant of the α2b-adrenoceptor is related to emotional memory in Europeans and Africans , 2007, Nature Neuroscience.

[53]  H. Eichenbaum.  Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[54]  Gabriele Lohmann,et al.  Critical comments on dynamic causal modelling , 2012, NeuroImage.

[55]  A. Aleman,et al.  Bidirectional information flow in frontoamygdalar circuits in humans: a dynamic causal modeling study of emotional associative learning. , 2012, Cerebral cortex.

[56]  Karl J. Friston,et al.  The Cortical Dynamics of Intelligible Speech , 2008, The Journal of Neuroscience.

[57]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[58]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[59]  Karl J. Friston,et al.  Dynamic causal modeling: A generative model of slice timing in fMRI , 2007, NeuroImage.

[60]  S. Rauch,et al.  Amygdala, Medial Prefrontal Cortex, and Hippocampal Function in PTSD , 2006, Annals of the New York Academy of Sciences.

[61]  Karl J. Friston.  Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[62]  J. Grafman,et al.  Focal brain damage protects against post-traumatic stress disorder in combat veterans , 2008, Nature Neuroscience.

[63]  J. D. McGaugh,et al.  Memory modulation. , 2011, Behavioral neuroscience.

[64]  Karl J. Friston,et al.  Slice-timing effects and their correction in functional MRI , 2011, NeuroImage.