Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording

doi:10.1006/nimg.2001.0904

NeuroImage

Volume 14, Issue 5, November 2001, Pages 1070-1079

https://doi.org/10.1006/nimg.2001.0904 Get rights and content

Abstract

The experience and appraisal of threat is essential to human and animal survival. Lesion evidence suggests that the subjective experience of fear relies upon amygdala-medial frontal activity (as well as autonomic arousal), whereas the factual context of threat stimuli depends upon hippocampal-lateral frontal activity. This amygdala-hippocampus dissociation has not previously been demonstrated in vivo. To explore this differentiation, we employed functional magnetic resonance imaging (fMRI) and simultaneous skin conductance response (SCR) measures of phasic arousal, while subjects viewed fearful versus neutral faces. fMRI activity was subaveraged according to whether or not the subject evoked an arousal SCR to each discrete face stimulus. The fMRI-with arousal and fMRI-without arousal data provided a distinct differentiation of amygdala and hippocampal networks. Amygdala-medial frontal activity was observed only with SCRs, whereas hippocampus-lateral frontal activity occurred only in the absence of SCRs. The findings provide direct evidence for a dissociation between human amygdala and hippocampus networks in the visceral experience versus declarative fact processing of fear.

References (47)

F. Aboitiz et al.
The evolutionary origin of the language areas in the human brain: A neuroanatomical perspective
Brain Res. Rev.
(1997)
M.J. Brammer et al.
Generic brain activation mapping in functional magnetic resonance imaging: A nonparametric approach
Magn. Reson. Imag.
(1997)
C. Buchel et al.
Brain systems mediating aversive conditioning: An event-related fMRI study
Neuron
(1998)
G. Bush et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends Cogn. Sci.
(2000)
J.E. LeDoux
Emotional memory systems in the brain
Behav. Brain. Res.
(1993)
CL. Lim et al.
Decomposing skin conductance into tonic and phasic components
Int. J Psychophysiol.
(1997)
M.L. Phillips et al.
A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics
Psychiatry Res. Neuroimag.
(1999)
J.D. Schmahmann
The role of the cerebellum in affect and psychosis
J. Neuroling.
(2000)
R. Adolphs et al.
Impaired recognition of facial expressions following bilateral damage to the human amygdala
Nature
(1994)
H. Bahramali et al.
Evoked related potentials associated with and without an orienting reflex
NeuroReport
(1997)

R.J. Barry et al.

Habituation of phasic and tonic components of the Orienting Reflex

Int. J. Psychophysiol.

(1993)

A. Bechara et al.

Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans

Science

(1995)

D.L. Bihan et al.

Applications of magnetic resonance imaging to the study of human brain function

Curr. Opin. Neurobiol.

(1995)

W. Boucsein

Electrodermal Activity

(1992)

H.C. Brieter et al.

Response and habituation of the human amygdala during visual processing of facial expression

Neuron

(1996)

E. Bullmore et al.

Functional MR imaging of confounded hypofrontality

Hum. Brain Mapp.

(1999)

E. Bullmore et al.

Coloured noise and computational inference in neuropsychological (fMRI) time series analysis: Resampling methods in time an wavelet domains

Hum. Brain Mapp.

(2001)

T.J. Bussey et al.

Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat—Implications for the neurobiology of emotion

Behav. Neurosci.

(1997)

A. Calder et al.

Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear

Cogn. Neuropsychol.

(1996)

A.J. Calder et al.

Computer-enhanced emotion in facial expressions

Proc. R. Soc. Lond.

(1997)

H.D. Critchley et al.

Neural activity relating to generation and representation of galvanic skin conductance responses: A functional magnetic resonance imaging study

J. Neurosci.

(2000)

A.R. Damasio

The somatic marker hypothesis and the possible functions of the prefrontal cortex

Phil. Trans. R. Soc. Lond.

(1996)

R.J. Davidson et al.

Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience

Psychol. Bull.

(2000)

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Regular ArticleArousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording

Abstract

Brain Res. Rev.

Magn. Reson. Imag.

Neuron

Trends Cogn. Sci.

Behav. Brain. Res.

Int. J Psychophysiol.

Psychiatry Res. Neuroimag.

J. Neuroling.

Impaired recognition of facial expressions following bilateral damage to the human amygdala

Nature

Evoked related potentials associated with and without an orienting reflex

NeuroReport

Habituation of phasic and tonic components of the Orienting Reflex

Int. J. Psychophysiol.

Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans

Science

Applications of magnetic resonance imaging to the study of human brain function

Curr. Opin. Neurobiol.

Electrodermal Activity

Response and habituation of the human amygdala during visual processing of facial expression

Neuron

Functional MR imaging of confounded hypofrontality

Hum. Brain Mapp.

Coloured noise and computational inference in neuropsychological (fMRI) time series analysis: Resampling methods in time an wavelet domains

Hum. Brain Mapp.

Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat—Implications for the neurobiology of emotion

Behav. Neurosci.

Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear

Cogn. Neuropsychol.

Computer-enhanced emotion in facial expressions

Proc. R. Soc. Lond.

Neural activity relating to generation and representation of galvanic skin conductance responses: A functional magnetic resonance imaging study

J. Neurosci.

The somatic marker hypothesis and the possible functions of the prefrontal cortex

Phil. Trans. R. Soc. Lond.

Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience

Psychol. Bull.

Regular Article
Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording