The Amygdala, the Hippocampus, and Emotional Modulation of Memory

There are two views regarding the role of the amygdala in emotional memory formation. According to one view, the amygdala modulates memory-related processes in other brain regions, such as the hippocampus. According to the other, the amygdala is a site for some aspects of emotional memory. Here the authors adduce behavioral, electrophysiological, and biochemical evidence in support of an integrative view, assuming both roles for the amygdala. This integrative view, however, suggests a level of complexity not referred to before: the assumption that emotional conditions induce long-term neural plasticity in the amygdala suggests that the interrelations between the amygdala and brain regions, such as the hippocampus, may not be static but dynamic. The way the amygdala will affect memory-related processes in the hippocampus may thus largely depend on the previous history of the individual.

[1]  Joseph E LeDoux,et al.  Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala , 1999, Neuron.

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

[3]  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.

[4]  S Levine,et al.  Behavioral stress impairs long-term potentiation in rodent hippocampus. , 1987, Behavioral and neural biology.

[5]  R P Kesner,et al.  Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. , 1994, Behavioral and neural biology.

[6]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[7]  Alex Pentland,et al.  Modeling and Prediction of Human Behavior , 1999, Neural Computation.

[8]  T. Dunwiddie,et al.  Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Michael Davis,et al.  Regulation of Synaptic Plasticity Genes during Consolidation of Fear Conditioning , 2002, The Journal of Neuroscience.

[10]  K. Abe Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. , 2001, Japanese journal of pharmacology.

[11]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[12]  C. Sandi,et al.  Differential activation of hippocampus and amygdala following spatial learning under stress , 2001, The European journal of neuroscience.

[13]  G. Richter-Levin,et al.  Mechanisms of Amygdala Modulation of Hippocampal Plasticity , 2002, The Journal of Neuroscience.

[14]  Carmen Sandi,et al.  Experience‐dependent Facilitating Effect of Corticosterone on Spatial Memory Formation in the Water Maze , 1997, The European journal of neuroscience.

[15]  Benno Roozendaal,et al.  Glucocorticoids and the regulation of memory consolidation , 2000, Psychoneuroendocrinology.

[16]  James L. McGaugh,et al.  Stress and glucocorticoids impair retrieval of long-term spatial memory , 1998, Nature.

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

[18]  D. Diamond,et al.  Inverted‐U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation , 1992, Hippocampus.

[19]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. , 1988, Brain research.

[20]  A. McDonald Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[21]  J. Fuster,et al.  Reactivity of limbic neurons of the monkey to appetitive and aversive signals. , 1971, Electroencephalography and clinical neurophysiology.

[22]  E. Kandel,et al.  Requirement of a critical period of transcription for induction of a late phase of LTP. , 1994, Science.

[23]  U. Frey,et al.  Different mechanisms and multiple stages of LTP. , 1990, Advances in experimental medicine and biology.

[24]  A. Pitkänen,et al.  Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat , 1999, The Journal of comparative neurology.

[25]  G M Rose,et al.  Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. , 1996, Behavioral neuroscience.

[26]  J. W. Rudy,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral neuroscience.

[27]  Karim Nader,et al.  Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective , 2001, Trends in Neurosciences.

[28]  G. Richter-Levin,et al.  Biphasic Modulation of Hippocampal Plasticity by Behavioral Stress and Basolateral Amygdala Stimulation in the Rat , 1999, The Journal of Neuroscience.

[29]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[30]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[31]  K. Obata,et al.  Identification of genes expressed in the amygdala during the formation of fear memory. , 2001, Learning & memory.

[32]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[33]  Torfi Sigurdsson,et al.  Long‐term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala , 2003, The European journal of neuroscience.

[34]  E. W. Kairiss,et al.  Long‐Term synaptic potentiation in the amygdala , 1990, Synapse.

[35]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[36]  Bruce S. McEwen,et al.  The effects of Type I and Type II corticosteroid receptor agonists on exploratory behavior and spatial memory in the Y-maze , 1997, Brain Research.

[37]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[38]  R Jaffard,et al.  Footshock stress but not contextual fear conditioning induces long‐term enhancement of auditory‐evoked potentials in the basolateral amygdala of the freely behaving rat , 1998, The European journal of neuroscience.

[39]  R. Anwyl,et al.  Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Blanchard,et al.  Ethoexperimental approaches to the biology of emotion. , 1988, Annual review of psychology.

[41]  M. Maroun,et al.  Exposure to Acute Stress Blocks the Induction of Long-Term Potentiation of the Amygdala–Prefrontal Cortex Pathway In Vivo , 2003, The Journal of Neuroscience.

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

[43]  Joseph E. LeDoux,et al.  LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit , 1995, Neuron.

[44]  Joseph E LeDoux,et al.  Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat , 1999, The Journal of comparative neurology.

[45]  Sanger Brown,et al.  An Investigation into the Functions of the Occipital and Temporal Lobes of the Monkey's Brain , 1888 .

[46]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[47]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[48]  M. Oitzl,et al.  Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. , 1992, Behavioral neuroscience.

[49]  J. D. McGaugh,et al.  Is the Amygdala a Locus of “Conditioned Fear”? Some Questions and Caveats , 1999, Neuron.

[50]  Y Watanabe,et al.  Effects of glucocorticoids on hippocampal long‐term potentiation , 1993, Hippocampus.

[51]  B. McEwen,et al.  Stress and cognitive function , 1995, Current Opinion in Neurobiology.

[52]  Joseph E LeDoux,et al.  A gradient of plasticity in the amygdala revealed by cortical and subcortical stimulation, in vivo , 2001, Neuroscience.

[53]  L. Swanson,et al.  Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: A PHAL anterograde tract‐tracing study in the rat , 1992, The Journal of comparative neurology.

[54]  David M. Diamond,et al.  The stressed hippocampus, synaptic plasticity and lost memories , 2002, Nature Reviews Neuroscience.

[55]  J. D. McGaugh,et al.  Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Joseph E LeDoux,et al.  Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[58]  D. Diamond,et al.  Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: mechanistic and temporal profiles , 2003, Neuroscience.

[59]  W. Abraham,et al.  Induction and Experience-Dependent Consolidation of Stable Long-Term Potentiation Lasting Months in the Hippocampus , 2002, The Journal of Neuroscience.

[60]  Gal Richter-Levin,et al.  Emotional tagging of memory formation—in the search for neural mechanisms , 2003, Brain Research Reviews.