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The human amygdala is involved in general behavioral relevance detection: Evidence from an event-related functional magnetic resonance imaging Go-NoGo task
Open accessAbstract
The amygdala is classically regarded as a detector of potential threat and as a critical component of the neural circuitry mediating conditioned fear responses. However, it has been reported that the human amygdala responds to multiple expressions of emotions as well as emotionally neutral stimuli of a novel, uncertain or ambiguous nature. Thus, it has been proposed that the function of the amygdala may be of a more general art, i.e. as a detector of behaviorally relevant stimuli [Sander D, Grafman J, Zalla T (2003) The human amygdala: an evolved system for relevance detection. Rev Neurosci 14:303-316]. To investigate this putative function of the amygdala, we used event related functional magnetic resonance imaging (fMRI) and a modified Go-NoGo task composed of behaviorally relevant and irrelevant letter and number stimuli. Analyses revealed bilateral amygdala activation in response to letter stimuli that were behaviorally relevant as compared with letters with less behavioral relevance. Similar results were obtained for relatively infrequent NoGo relevant stimuli as compared with more frequent Go stimuli. Our findings support a role for the human amygdala in general detection of behaviorally relevant stimuli.
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“Converging evidence from this field suggests the amygdalaa key brain region for emotion regulation (LeDoux, 2003), processing (Seeley et al., 2007), detection (Ousdal et al., 2008), and vigilance for social cues across sensory modalities (Whalen, 2007) is an important target of OT administration.”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Ousdal et al., 2008
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Cites
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“During the past several years the classical view of the amygdala as a threat detector/fear-module has been expanded following multiple reports linking the amygdala to non-fearful emotional facial expressions including happiness (Breiter et al., 1996; Morris et al., 1996; Canli et al., 2002), sadness (Blair et al.”
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“…has been expanded following multiple reports linking the amygdala to non-fearful emotional facial expressions including happiness (Breiter et al., 1996; Morris et al., 1996; Canli et al., 2002), sadness (Blair et al., 1999), contempt (Sambataro et al., 2006) and anger (Fitzgerald et al., 2006).”
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Herry, C., Bach, D. R., Esposito, F., Di Salle, F., Perrig, W. J., Scheffler, K., Lüthi, A., & Seifritz, E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5218-06.2007 · Cited by 401 · cited 2×
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Büchel, C. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00078-7 · Cited by 360 · cited 2×
“Further, patients with amygdala lesions showed blunted emotional responses during fear conditioning (Buchel and Dolan, 2000), a phenomenon also noted in Alzheimer's patients who have amygdala atrophy (Hamann et al., 2002).”
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“Macaques with amygdala lesions exhibit decreased fear of predators and diminished stress in novel social situations (Amaral, 2002; Emery et al., 2001), observations initially interpreted as supporting a unique role of the amygdala as danger/threat detector (Amaral, 2002).”
BackgroundWilliams, L. M., Phillips, M. L., Brammer, M. J., Skerrett, D., Lagopoulos, J., Rennie, C., Bahramali, H., Olivieri, G., David, A. S., Peduto, A., et al. (2001) · NeuroImage · doi:10.1006/nimg.2001.0904 · Cited by 300 · cited 2×
“(2008) found that rising sound intensity (signaling relevance) facilitated the autonomic orienting reflex and phasic alertness to auditory targets, responses believed to be mediated through the amygdala (Williams et al., 2001).”
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“Macaques with amygdala lesions exhibit decreased fear of predators and diminished stress in novel social situations (Amaral, 2002; Emery et al., 2001), observations initially interpreted as supporting a unique role of the amygdala as danger/threat detector (Amaral, 2002).”
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“Also, socially relevant stimuli without explicit emotional valence like novel, neutral faces (Schwartz et al., 2003a,b; Wright and Liu, 2006), untrustworthy faces (Winston et al., 2002; Engell et al., 2007), facial attractiveness (Winston et al., 2007) and eyegaze (Adams et al., 2003) as well as…”
BackgroundGoldstein, M., Brendel, G., Tüscher, O., Pan, H., Epstein, J., Beutel, M. E., Yang, Y., Thomas, K. F., Levy, K. N., Silverman, M. E., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.01.056 · Cited by 215 · cited 2×
“Goldstein et al. (2007) created relevant stimuli using goalrelevance manipulation in an emotional linguistic Go/NoGo task.”
MethodKiehl, K. A., & Liddle, P. F. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00117-1 · Cited by 214 · cited 4×
“Amygdala has been shown to respond to target stimuli in auditory oddball paradigm (Kiehl and Liddle, 2001), still one cannot be certain that this response is due to the behavioral relevance of the targets or the motor response to these per se, as the other stimuli often do not require button…”
BackgroundResultInfluentialRising sound intensity: an intrinsic warning cue activating the amygdala.
Bach, D., Schächinger, H., Neuhoff, J. G., Esposito, F., Salle, F. D., Lehmann, C., Herdener, M., Scheffler, K., & Seifritz, E. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm040 · Cited by 181 · cited 3×
“, 2003) and rising sound intensity (Bach et al., 2008).”
BackgroundImpaired fear conditioning in Alzheimer’s disease
Hamann, S., Monarch, E. S., & Goldstein, F. C. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00223-8 · Cited by 129 · cited 1×
“Further, patients with amygdala lesions showed blunted emotional responses during fear conditioning (Buchel and Dolan, 2000), a phenomenon also noted in Alzheimer's patients who have amygdala atrophy (Hamann et al., 2002).”
BackgroundSelective bilateral amygdala lesions in rhesus monkeys fail to disrupt object reversal learning
Izquierdo, A., & Murray, E. A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3616-06.2007 · Cited by 121 · cited 2×
“After discovering that such lesions also impair food devaluation, the amygdala’s role was extended to reward-related processes ( Izquierdo and Murray, 2007 ).”
BackgroundIndividual Differences in Amygdala Activity Predict Response Speed during Working Memory
Schaefer, A., Braver, T. S., Reynolds, J. R., Burgess, G. C., Yarkoni, T., & Gray, J. R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2567-06.2006 · Cited by 106 · cited 2×
“Our current results are consistent with those recently reported by Schaefer et al. (2006) , who demonstrated that individual differences in response speed during a three-back working memory task with non-emotional stimuli was correlated with magnitude of amygdala activity.”
ResultSchirmer, A., Escoffier, N., Zysset, S., Koester, D., Striano, T., & Friederici, A. D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.01.018 · Cited by 95 · cited 2×
“According to Schirmer et al. (2008), social orientation correlated with amygdala activity elicited by emotional vocalization, so that subjects interested in social exchange had significantly larger amygdala responses to emotional vocalization than those less interested.”
BackgroundNeutral faces activate the amygdala during identity matching
Wright, P. K., & Liu, Y. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.07.047 · Cited by 88 · cited 2×
“Also, socially relevant stimuli without explicit emotional valence like novel, neutral faces (Schwartz et al., 2003a,b; Wright and Liu, 2006), untrustworthy faces (Winston et al., 2002; Engell et al., 2007), facial attractiveness (Winston et al., 2007) and eyegaze (Adams et al., 2003) as well as…”
BackgroundPreferential responses in amygdala and insula during presentation of facial contempt and disgust
Sambataro, F., Dimalta, S., Giorgio, A. D., Taurisano, P., Blasi, G., Scarabino, T., Giannatempo, G. M., Nardini, M., & Bertolino, A. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05120.x · Cited by 74 · cited 2×
“…has been expanded following multiple reports linking the amygdala to non-fearful emotional facial expressions including happiness (Breiter et al., 1996; Morris et al., 1996; Canli et al., 2002), sadness (Blair et al., 1999), contempt (Sambataro et al., 2006) and anger (Fitzgerald et al., 2006).”
BackgroundA supramodal limbic‐paralimbic‐neocortical network supports goal‐directed stimulus processing
Laurens, K. R., Kiehl, K. A., & Liddle, P. F. (2004) · Human Brain Mapping · doi:10.1002/hbm.20062 · Cited by 58 · cited 2×
“those not requiring responses) is further supported by findings of greater amygdala activity to “oddball” target stimuli (Kiehl and Liddle, 2001) as well as to Go events in an emotionally neutral GoNoGo task (Laurens et al., 2005).”
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“Fourth, a central challenge will be to determine whether increased MCC control signals are a consequence of amplified punishment-related information arriving from distal brain regions, such as the extended amygdala (Brázdil et al., 2002; Nishijo et al., 2008; Ousdal et al., 2008), or instead reflect local changes in t…”
Implicit Trustworthiness Decisions: Automatic Coding of Face Properties in the Human Amygdala
Engell, A. D., Haxby, J. V., & Todorov, A. T. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.9.1508 · Cited by 489
Bzdok, D., Laird, A. R., Zilles, K., Fox, P. T., & Eickhoff, S. B. (2012) · Human Brain Mapping · doi:10.1002/hbm.22138 · Cited by 450
“Newer evidence, however, extended this concept to the extraction of biological significance from the environment [Sander et al., 2003] and the consequent shaping of behavioral responses [Ousdal et al., 2008].”
BackgroundCriaud, M., & Boulinguez, P. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.11.003 · Cited by 368
Metadata
- Authors
- Ousdal, O. T., Jensen, J., Server, A., Hariri, A. R., Nakstad, P. H., & Andreassen, O. A.
- Affiliations
- Oslo University Hospital (NO)
- University of Oslo (NO)
- University of Pittsburgh (US)
- Corresponding author
- Andreassen, O.A.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2008-10
- Volume
- 156
- Issue
- 3
- Pages
- 450-455
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC2755288
- OpenAlex
- W2004180312
- Cited by
- 102
- References
- 45
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 5 · 2018: 3 · 2017: 2 · 2016: 3 · 2015: 7 · 2014: 8 · 2013: 9 · 2012: 15
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Universitetet i Oslo
- Norges Forskningsråd (#167153/V50, #163070/V50, 167153)
- National Institute of Mental Health (K01MH072837)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- amygdala, go/no-go task, emotional salience, threat detection, stimulation frequency
- MeSH terms
- Adult, Amygdala, Decision Making, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Oxygen, Pattern Recognition, Visual, Photic Stimulation, Reaction Time, Signal Detection, Psychological, Young Adult
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