Linguistic threat activates the human amygdala.

Studies in animals demonstrate a crucial role for the amygdala in emotional and social behavior, especially as related to fear and aggression. Whereas lesion and functional-imaging studies in humans indicate the amygdala's participation in assessing the significance of nonverbal as well as paralinguistic cues, direct evidence for its role in the emotional processing of linguistic cues is lacking. In this study, we use a modified Stroop task along with a high-sensitivity neuroimaging technique to target the neural substrate engaged specifically when processing linguistic threat. Healthy volunteer subjects were instructed to name the color of words of either threat or neutral valence, presented in different color fonts, while neural activity was measured by using H(2)(15)O positron-emission tomography. Bilateral amygdalar activation was significantly greater during color naming of threat words than during color naming of neutral words. Associated activations were also noted in sensory-evaluative and motor-planning areas of the brain. Thus, our results demonstrate the amygdala's role in the processing of danger elicited by language. In addition, the results reinforce the amygdala's role in the modulation of the perception of, and response to, emotionally salient stimuli. The current study further suggests conservation of phylogenetically older mechanisms of emotional evaluation in the context of more recently evolved linguistic function.

[1]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[2]  F. Reinoso-suárez,et al.  Amygdaloid projections to prefrontal and motor cortex. , 1977, Science.

[3]  J. Winn,et al.  Brain , 1878, The Lancet.

[4]  E. Halgren,et al.  Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. , 1978, Brain : a journal of neurology.

[5]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[6]  Rolls Et Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. , 1984 .

[7]  E. Rolls,et al.  Neurons in the amygdala of the monkey with responses selective for faces , 1985, Behavioural Brain Research.

[8]  E. Halgren,et al.  Neural encoding of individual words and faces by the human hippocampus and amygdala , 1988, Nature.

[9]  N. J. Cohen,et al.  Is There a Special Flashbulb-Memory Mechanism? , 1988 .

[10]  P Gloor,et al.  Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. , 1990, Brain : a journal of neurology.

[11]  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.

[12]  P. Eslinger The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction edited by J.P. Aggleton, Wiley-Liss, 1992. $125.00 (xii + 615 pages) ISBN 0 4715 6129 0 , 1992, Trends in Neurosciences.

[13]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[14]  Richard S. J. Frackowiak,et al.  Detection of Thirty-Second Cognitive Activations in Single Subjects with Positron Emission Tomography: A New Low-Dose H215O Regional Cerebral Blood Flow Three-Dimensional Imaging Technique , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  K. Perrine,et al.  Neurobehavioral problems in epilepsy. , 1994, Neurologic clinics.

[16]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[17]  B. J. Casey,et al.  Regional brain activity when selecting a response despite interference: An H2 15O PET study of the stroop and an emotional stroop , 1994, Human brain mapping.

[18]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[19]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  M. McDaniel,et al.  The bizarreness effect: it's not surprising, it's complex. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[21]  D. Hedeker,et al.  MIXREG: a computer program for mixed-effects regression analysis with autocorrelated errors. , 1996, Computer methods and programs in biomedicine.

[22]  A. Chiba,et al.  The amygdala and emotion , 1996, Current Opinion in Neurobiology.

[23]  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.

[24]  Sophie K. Scott,et al.  Impaired auditory recognition of fear and anger following bilateral amygdala lesions , 1997, Nature.

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

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

[27]  R. Haier,et al.  Hippocampal, but not amygdala, activity at encoding correlates with long-term, free recall of nonemotional information. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

[29]  S. Kuriki,et al.  Neural processing of words in the human extrastriate visual cortex. , 1998, Brain research. Cognitive brain research.

[30]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[31]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[32]  A K Anderson,et al.  Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. , 1998, Neuroreport.

[33]  James T. Becker,et al.  Functional Neuroanatomy of Semantic Memory: Recognition of Semantic Associations , 1999, NeuroImage.

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