The Human Amygdala: An Evolved System for Relevance Detection
Abstract
Evidence from pioneering animal research has suggested that the amygdala is involved in the processing of aversive stimuli, particularly fear-related information. Fear is central in the evolution of the mammalian brain: it is automatically and rapidly elicited by potentially dangerous and deadly events. The view that the amygdala shares the main characteristics of modular systems, e.g. domain specificity, automaticity, and cognitive impenetrability, has become popular in neuroscience. Because of its computational properties, it has been proposed to implement a rapid-response 'fear module'. In this article, we review recent patient and neuroimaging data of the human brain and argue that the fundamental criteria for the amygdala to be a modular system are not met. We propose a different computational view and suggest the notion of a specific involvement of the human amygdala in the appraisal of relevant events that include, but are not restricted to, fear-related stimuli. Considering the amygdala as a 'relevance detector' would integrate the 'fear module' hypothesis with the concept of an evolved neural system devoted to the processing of a broader category of biologically relevant stimuli. In primates, socially relevant events appear to have become, through evolution, the dominant elements of the amygdala's domain of specificity.
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The AM is thought to automatically extract biological significance from the environment.
“This brain region is thought to automatically extract biological significance from the environment (Ball et al. 2007; Sander et al. 2003; Bzdok et al. 2011; Müller et al. 2011).”
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Small, D. M., Veldhuizen, M. G., Felsted, J. A., Mak, Y. E., & McGlone, F. P. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.021 · Cited by 190 · see citing works
ALE meta-analysis on facial judgments of trustworthiness and attractiveness
Bzdok, D., Langner, R., Caspers, S., Kurth, F., Habel, U., Zilles, K., Laird, A., & Eickhoff, S. B. (2011) · Brain Structure and Function · doi:10.1007/s00429-010-0287-4 · Cited by 183 · see citing works
Ball, T., Rahm, B., Eickhoff, S. B., Schulze-Bonhage, A., Speck, O., & Mutschler, I. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000307 · Cited by 176 · see citing works
“The challenge of unraveling the function of the human amygdala is attracting great interest [1–5].”
BackgroundThe social evaluation of faces: a meta-analysis of functional neuroimaging studies
Mende‐Siedlecki, P., Said, C. P., & Todorov, A. T. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr090 · Cited by 175 · see citing works
N’Diaye, K., Sander, D., & Vuilleumier, P. O. (2009) · Emotion · doi:10.1037/a0017845 · Cited by 176 · see citing works
“We predicted that the amygdala should show selective modulations depending on eye gaze direction, with angry faces producing greater responses with a direct than averted gaze, but fearful faces conversely producing greater responses with averted than direct gaze (Sander et al., 2003).”
InfluentialSelf-citationGerber, A. J., Posner, J. E., Gorman, D. A., Colibazzi, T., Yu, S., Wang, Z., Kangarlu, A., Hongtu Zhu, B., Russell, J. A., & Peterson, B. S. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.02.032 · Cited by 176 · see citing works
Altered neural reward and loss processing and prediction error signalling in depression
Ubl, B., Kuehner, C., Kirsch, P., Ruttorf, M., Diener, C., & Flor, H. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu158 · Cited by 165 · see citing works
“…2011), and attention is primarily attracted by salient (or alerting) stimuli, several studies emphasise the role of the amygdala in the detection and evaluation of stimuli that are motivationally significant for behaviour (Sander et al., 2003; Herbert et al., 2009; Cunningham and Kirkland, 2013).”
BackgroundRising Sound Intensity: An Intrinsic Warning Cue Activating the Amygdala
Bach, D. R., Schächinger, H., Neuhoff, J. G., Esposito, F., Salle, F. D., Lehmann, C., Herdener, M., Scheffler, K., & Seifritz, E. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm040 · Cited by 180 · see citing works
“2006), relevance (Sander et al. 2003), and ambiguity (Whalen 1998; Rosen and Donley 2006).”
BackgroundInfluentialAmygdala and heart rate variability responses from listening to emotionally intense parts of a story
Wallentin, M., Højlund, A., Vuust, P., Dohn, A., Roepstorff, A., & Lund, T. E. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.06.077 · Cited by 172 · see citing works
“Recent developments within the study of emotional processing, however, have suggested that rather than being a fear “module”, these pathways may constitute a more general system for relevance detection (Herbert et al., 2009; Paton et al., 2006; Sander et al., 2003; Sergerie et al., 2008) monitoring both positive and n…”
Background5-HTTLPR Biases Amygdala Activity in Response to Masked Facial Expressions in Major Depression
Dannlowski, U., Ohrmann, P., Bauer, J., Deckert, J., Hohoff, C., Kugel, H., Arolt, V., Heindel, W. L., Kersting, A., Baune, B. T., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301411 · Cited by 173 · see citing works
How do we know the minds of others? Domain-specificity, simulation, and enactive social cognition
Adolphs, R. (2006) · Brain Research · doi:10.1016/j.brainres.2005.12.127 · Cited by 170 · see citing works
“Domain-specificity, simulation, and enactive social cognition”
ResultAnosognosia for hemiplegia: a clinical-anatomical prospective study
Vocat, R., Staub, F., Stroppini, T., & Vuilleumier, P. O. (2010) · Brain · doi:10.1093/brain/awq297 · Cited by 171 · see citing works
“The amygdala is a structure critically implicated in emotional processing and learning (see Phelps and LeDoux, 2005 for a review), with a particular importance for fear (Ohman and Mineka, 2001) and, more generally, for the appraisal of self-relevant stimuli (Sander et al., 2003).”
BackgroundNeural correlates of automatic beliefs about gender and race
Knutson, K. M., Mah, L., Manly, C. F., & Grafman, J. H. (2006) · Human Brain Mapping · doi:10.1002/hbm.20320 · Cited by 168 · see citing works
“Gender discrimination/stereotyping tasks may be some of the functions of the amygdala, which in general include providing a quick, unconscious, affect- [Cunningham et al., 2003] and relevance-based [Sander et al., 2003] evaluation of the environment that prepares one for immediate action.”
BackgroundSelf-citationGerdes, A. B. M., Wieser, M. J., & Alpers, G. W. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01351 · Cited by 169 · see citing works
“…December 2014 | Volume 5 | Article 1351 | 1 cues and has been documented to operate independently from the sensory modality which conveyed the information (Armony and LeDoux, 2000; Sander et al., 2003; Zald, 2003; Öhman, 2005; Stekelenburg and Vroomen, 2007; Scharpf et al., 2010; Armony, 2013).”
BackgroundAllocation of spatial attention to emotional stimuli depends upon arousal and not valence.
Vogt, J., Houwer, J. D., Koster, E. H. W., Damme, S. V., & Crombez, G. (2008) · Emotion · doi:10.1037/a0013981 · Cited by 167 · see citing works
Structural neuroplasticity in expert pianists depends on the age of musical training onset
Vaquero, L., Hartmann, K., Ripollés, P., Rojo, N., Sierpowska, J., François, C., Càmara, E., Vugt, F. T., Mohammadi, B., Samii, A., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2015.11.008 · Cited by 136 · see citing works
“Human studies suggest that the amygdala is not restricted to the processing of emotional or fear-related stimuli, but that it has a broader role in the detection of relevant stimuli (Sander et al., 2003), which might be important during the music-learning process.”
Emotional States from Affective Dynamics
Cunningham, W. A., Dunfield, K. A., & Stillman, P. E. (2013) · Emotion Review · doi:10.1177/1754073913489749 · Cited by 158 · see citing works
The embodied brain: towards a radical embodied cognitive neuroscience
Kiverstein, J. D., & Miller, M. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00237 · Cited by 168 · see citing works
“…about the amygdala in this regard, an area that is often referred to as supporting a discrete theory of fear because it has repeatedly been shown to be involved in threat responses in rats and humans (see e.g., LeDoux, 1996; Öhman and Mineka, 2001; for critical discussion see Sander et al., 2003).”
BackgroundBrain systems underlying the affective and social monitoring of actions: An integrative review
Koban, L., & Pourtois, G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.02.014 · Cited by 159 · see citing works
“…role of the amygdala in the detection of emotionally salient external stimuli (Anderson and Phelps, 2000; LaBar et al., 1998; Phelps, 2006; Sander et al., 2003; Vuilleumier, 2005; Whalen et al., 2001), this structure could be similarly involved in the rapid affective monitoring of…”
Diekhof, E. K., Falkai, P., & Gruber, O. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.07.004 · Cited by 165 · see citing works
Amygdala activation during reading of emotional adjectives--an advantage for pleasant content.
Herbert, C., Ethofer, T., Anders, S., Junghöfer, M., Wildgruber, D., Grodd, W., & Kissler, J. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn027 · Cited by 159 · see citing works
“It 5 alerts us in principle towards both hostile and pleasurable stimuli but takes into account internal milieu states as well as current environmental and individual demands (Sander et al., 2003).”
BackgroundResultInfluentialAmygdalohippocampal involvement in tinnitus and auditory memory
Ridder, D. D., Fransen, H., Francois, O., Sunaert, S. G., Kovacs, S., & de Heyning, P. V. (2006) · Acta Oto-Laryngologica · doi:10.1080/03655230600895580 · Cited by 160 · see citing works
van de Riet, W. A. C., Grèzes, J., & de Gelder, B. (2009) · Social Neuroscience · doi:10.1080/17470910701865367 · Cited by 159 · see citing works
- Authors
- Sander, D., Grafman, J., & Zalla, T.
- Affiliations
- University of Geneva (CH)
- National Institutes of Health (US)
- Institut des Sciences Cognitives (FR)
- Venue
- Reviews in the Neurosciences
- Publisher
- Walter de Gruyter GmbH
- Published
- 2003-01
- Volume
- 14
- Issue
- 4
- Pages
- 303-16
- ISSN
- 0334-1763 (ISSN-L)
- 2191-0200
- OpenAlex
- W2290816323
- Cited by
- 944
- References
- 2
- Citations by year
- 2026: 11 · 2025: 22 · 2024: 34 · 2023: 45 · 2022: 37 · 2021: 43 · 2020: 47 · 2019: 55 · 2018: 45 · 2017: 60 · 2016: 42 · 2015: 69 · 2014: 48 · 2013: 75 · 2012: 81
- FWCI
- 5.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reviews in the Neurosciences (publishedVersion)
- PubMed (publishedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion)
- Funders
- University of Arizona
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- human amygdala, relevance detection, modularity of mind, domain specificity, automaticity, evolutionary neuroscience, social relevance, fear processing
- MeSH terms
- Amygdala, Animals, Computers, Emotions, Biological Evolution, Humans, Magnetic Resonance Imaging, Mental Processes, Models, Neurological, Systems Theory, Signal Detection, Psychological
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