Extended Amygdala and Emotional Salience: A PET Activation Study of Positive and Negative Affect

Functional neuroimaging studies have implicated amygdaloid and basal forebrain regions, including sublenticular extended amygdala (SLEA), in the mediation of aversive emotional responses. However, it is not clear whether SLEA responds to ‘aversiveness’ or to general stimulus salience. We predicted that both pleasant and aversive stimuli would activate this region. Using [15O] water PET, we studied 10 healthy subjects while viewing pleasant, aversive, neutral, and blank images. Each subject underwent eight scans, which were processed and averaged with standard statistical methods. Both positive and negative stimuli activated regions in SLEA. Both positive and negative content activated the visual cortex, relative to neutral content. Aversive stimuli deactivated the left frontal pole, relative to positive and neutral stimuli. These findings demonstrate that both positive and negative emotional content evokes processing in the sublenticular/extended amygdala region, suggesting that this region is involved in general emotional processing, such as detection or attribution of salience.

[1]  J. E. Holmes,et al.  Electrical activity of the cat amygdala during sexual behavior. , 1973, Physiology & behavior.

[2]  N. Geschwind,et al.  Hemispheric asymmetry in the expression of positive and negative emotions. Neurologic evidence. , 1982, Archives of neurology.

[3]  R. Gur,et al.  Hemispheric asymmetries in processing emotional expressions , 1983, Neuropsychologia.

[4]  Michael Davis,et al.  Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. , 1986, Behavioral neuroscience.

[5]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[6]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  Michael Davis,et al.  The role of the amygdala in conditioned fear. , 1992 .

[10]  S Minoshima,et al.  An automated method for rotational correction and centering of three-dimensional functional brain images. , 1992, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

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

[12]  A. Kling.  The amygdala and social behavior. , 1992 .

[13]  M. Mintun,et al.  Integrated and automated data analysis method for neuronal activation studies using O-15 water PET , 1993 .

[14]  Simon R. Cherry,et al.  Improved signal-to-noise in activation studies by exploiting the kinetics of oxygen-15 labeled water , 1993 .

[15]  Simon R. Cherry,et al.  Improved Detection of Focal Cerebral Blood Flow Changes Using Three-Dimensional Positron Emission Tomography , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[16]  R. Koeppe,et al.  Anatomic standardization: linear scaling and nonlinear warping of functional brain images. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[17]  R. Davidson.  Cerebral asymmetry, emotion, and affective style. , 1995 .

[18]  C H Beck,et al.  Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Y. Kondo,et al.  The possible involvement of the nonstrial pathway of the amygdala in neural control of sexual behavior in male rats , 1995, Brain Research Bulletin.

[20]  R. Dolan,et al.  Neural Activation during Covert Processing of Positive Emotional Facial Expressions , 1996, NeuroImage.

[21]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[22]  K. Berridge.  Food reward: Brain substrates of wanting and liking , 1996, Neuroscience & Biobehavioral Reviews.

[23]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  S. Kosslyn,et al.  Neural effects of visualizing and perceiving aversive stimuli: a PET investigation. , 1996, Neuroreport.

[25]  R. W. Flint,et al.  Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys. , 1996, Behavioral neuroscience.

[26]  Karl J. Friston,et al.  Neural responses to salient visual stimuli , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[28]  L. Heimer,et al.  Substantia innominata: a notion which impedes clinical–anatomical correlations in neuropsychiatric disorders , 1997, Neuroscience.

[29]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[30]  R E Harlan,et al.  The accumbens: beyond the core-shell dichotomy. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[31]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[32]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

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

[34]  W. Drevets,et al.  Functional neuroimaging studies of depression: the anatomy of melancholia. , 1998, Annual review of medicine.

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

[36]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[37]  Jeff T. Larsen,et al.  Negative information weighs more heavily on the brain: the negativity bias in evaluative categorizations. , 1998, Journal of personality and social psychology.

[38]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[39]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[40]  R. Roth,et al.  Engagement in a non‐escape (displacement) behavior elicits a selective and lateralized suppression of frontal cortical dopaminergic utilization in stress , 1999, Synapse.

[41]  Mitsuo Nakamura,et al.  Neural systems for behavioral activation and reward , 1999, Current Opinion in Neurobiology.

[42]  P. Holland,et al.  Amygdala circuitry in attentional and representational processes , 1999, Trends in Cognitive Sciences.

[43]  H. Breiter,et al.  Functional Magnetic Resonance Imaging of Brain Reward Circuitry in the Human , 1999, Annals of the New York Academy of Sciences.

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

[45]  S. Paradiso,et al.  Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. , 1999, The American journal of psychiatry.

[46]  L. Heimer,et al.  The Concepts of the Ventral Striatopallidal System and Extended Amygdala , 1999, Annals of the New York Academy of Sciences.

[47]  G. Schoenbaum,et al.  Functions of the Amygdala and Related Forebrain Areas in Attention and Cognition , 1999, Annals of the New York Academy of Sciences.

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

[49]  A. Sirigu,et al.  Differential amygdala responses to winning and losing: a functional magnetic resonance imaging study in humans , 2000, The European journal of neuroscience.

[50]  G. Koob.  Neurobiology of Addiction: Toward the Development of New Therapies , 2000, Annals of the New York Academy of Sciences.

[51]  A. Rasia-Filho,et al.  Functional activities of the amygdala: an overview. , 2000, Journal of psychiatry & neuroscience : JPN.

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

[53]  S. Taylor,et al.  Limbic Activation and Psychophysiologic Responses to Aversive Visual Stimuli: Interaction with Cognitive Task , 2000, Neuropsychopharmacology.

[54]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[55]  S. Taylor,et al.  The effect of graded aversive stimuli on limbic and visual activation , 2000, Neuropsychologia.

[56]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[57]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  H. Barbas,et al.  Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey , 2001, Neuroscience.

[59]  K. Berridge,et al.  Fear and Feeding in the Nucleus Accumbens Shell: Rostrocaudal Segregation of GABA-Elicited Defensive Behavior Versus Eating Behavior , 2001, The Journal of Neuroscience.

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