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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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“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).”
From Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy (2012) · cites this paper as Sander et al. 2003
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Unresolved trauma in mothers: intergenerational effects and the role of reorganization.
Iyengar, U., Kim, S., Martinez, S., Fonagy, P., & Strathearn, L. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00966 · Cited by 83
Humans Process Dog and Human Facial Affect in Similar Ways
Schirmer, A., Seow, C. S., & Penney, T. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074591 · Cited by 83
“Moreover, the amygdala has been construed as a relevance detector that responds to emotional human faces because it identifies their structural configuration as potentially important for the observer [34].”
BackgroundBernat, E. M., Cadwallader, M., Seo, D., Vizueta, N., & Patrick, C. J. (2011) · Developmental Neuropsychology · doi:10.1080/87565641.2010.549881 · Cited by 83
Neural networks related to dysfunctional face processing in autism spectrum disorder
Nickl‐Jockschat, T., Rottschy, C., Thommes, J., Schneider, F. W., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0791-z · Cited by 85
“of biological significance from the environment (Sander et al. 2003) and the shaping of behavioral responses (Ousdal et al.”
BackgroundThe amygdala and the relevance detection theory of autism: an evolutionary perspective
Zalla, T., & Sperduti, M. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00894 · Cited by 98
“Baron-Cohen et al. (2000) posited that damage or dysfunction of the amygdala should be at the root of social impairments in ASDs and proposed the Amygdala Theory of Autism.”
BackgroundMethodInfluentialSelf-citationFu, X., & Pérez‐Edgar, K. E. (2018) · Developmental Review · doi:10.1016/j.dr.2018.11.002 · Cited by 92
Brain Networks of Emotional Prosody Processing
Grandjean, D. (2020) · Emotion Review · doi:10.1177/1754073919898522 · Cited by 93
Neural responses to facial expressions support the role of the amygdala in processing threat
Mattavelli, G. C., Sormaz, M., Flack, T. R., Asghar, A. U. R., Fan, S., Frey, J. N., Manssuer, L. R., Usten, D., Young, A. W., & Andrews, T. J. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst162 · Cited by 88
“The alternative is that the amygdala has a more general role in emotional appraisal for which fear and likely anger, as suggested from our data, are the most effective elicitors (Sander et al., 2003).”
BackgroundAmygdala involvement in human avoidance, escape and approach behavior
Schlund, M. W., & Cataldo, M. F. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.058 · Cited by 81
“…of these conditions provided a novel opportunity to compare amygdala responses under a range of aversive and appetitive conditions to determine if it serves a broader role as a " behavioral relevance " detector (Ousdal et al., 2008; Paton et al., 2006; Sander et al, 2003; Schoenbaum et al., 2003).”
Explicit and Implicit Emotion Processing in the Cerebellum: A Meta-analysis and Systematic Review
Pierce, J. E., Thomasson, M., Voruz, P., Selosse, G., & Péron, J. (2022) · The Cerebellum · doi:10.1007/s12311-022-01459-4 · Cited by 88
“Yet most studies focused on the role of the amygdala or prefrontal cortex in generating or regulating emotional responses [17, 20, 41, 53, 59, 84].”
BackgroundAutonomic reactions indicating positive affect during acoustic reward learning in domestic pigs
Zebunke, M., Langbein, J., Manteuffel, G., & Puppe, B. (2010) · Animal Behaviour · doi:10.1016/j.anbehav.2010.11.023 · Cited by 82
“Some studies in humans and pigs have shown that one structure fulfilling this relevance detection is the amygdala (Sander et al. 2003; Ousdal et al. 2008; Kalbe & Puppe 2010).”
BackgroundThe role of the amygdala in face perception and evaluation
Todorov, A. T. (2011) · Motivation and Emotion · doi:10.1007/s11031-011-9238-5 · Cited by 85
“This proposal is consistent with several other proposals about the role of the amygdala in maintaining vigilance (Whalen 2007) and detection of salient or motivationally relevant stimuli (Adolphs 2010; Sander et al. 2003).”
ResultHeany, S. J., Groenewold, N. A., Uhlmann, A., Dalvie, S., Stein, D. J., & Brooks, S. J. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001717 · Cited by 87
Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys
Taubert, J., Flessert, M., Wardle, S. G., Basile, B. M., Murphy, A. P., Murray, E. A., & Ungerleider, L. G. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807245115 · Cited by 80
A Multidimensional Approach to Apathy after Traumatic Brain Injury
Arnould, A., Rochat, L., Azouvi, P., & der Linden, M. V. (2013) · Neuropsychology Review · doi:10.1007/s11065-013-9236-3 · Cited by 94
“More specifically, the amygdala is considered as a system for relevance detection, i.e., necessary for detecting the extent to which stimulus events are relevant for the current needs, goals and values of the individual (Sander et al. 2003; Ousdal et al. 2008).”
BackgroundConsidering PTSD from the perspective of brain processes: A psychological construction approach
Suvak, M. K., & Barrett, L. F. (2011) · Journal of Traumatic Stress · doi:10.1002/jts.20618 · Cited by 78
“A P S Y C H O L O G I C A L C O N S T R U C T I O N A P P R O A C H T O P T S D”
BackgroundFear across the senses: brain responses to music, vocalizations and facial expressions
Aubé, W., Angulo‐Perkins, A., Peretz, I., Concha, L., & Armony, J. L. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu067 · Cited by 85
“Others posit that the amygdala act as a relevance detector to biologically salient information (Sander et al., 2003) or even to ‘potential’ (but not necessarily actual) relevant stimuli (for a review, see Armony, 2013).”
BackgroundLevens, S. M., & Phelps, E. A. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21428 · Cited by 83
Emotions amplify speaker–listener neural alignment
Smirnov, D., Saarimäki, H., Glerean, E., Hari, R., Sams, M., & Nummenmaa, L. (2019) · Human Brain Mapping · doi:10.1002/hbm.24736 · Cited by 71
Amygdala subregions differentially respond and rapidly adapt to threatening voices
Frühholz, S., & Grandjean, D. (2012) · Cortex · doi:10.1016/j.cortex.2012.08.003 · Cited by 76
“Introduction 2005; Sander et al., 2005a; Wiethoff et al., 2009) or nonverbal The amygdala is an important brain structure for detecting the affective information (Zald, 2003) that is most relevant for the current context of behavior (Sander et al., 2003).”
Neurocognitive mechanisms of gaze-expression interactions in face processing and social attention
Graham, R., & LaBar, K. S. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.01.019 · Cited by 81
Yoder, K. J., Porges, E. C., & Decety, J. (2014) · Human Brain Mapping · doi:10.1002/hbm.22712 · Cited by 78
“…but not limited to fear conditioning [Ledoux et al., 1990], social and emotional processing [Adolphs et al., 2002; Phelps and LeDoux, 2005; Sander et al., 2003], processing stimulus relevance for the goals and motivations of the perceiver [Cunningham and Brosch, 2012] and the development…”
BackgroundEffects of emotional prosody on auditory extinction for voices in patients with spatial neglect
Grandjean, D., Sander, D., Lucas, N., Scherer, K. R., & Vuilleumier, P. O. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.08.025 · Cited by 72
Self-citationIf it bleeds, it leads: separating threat from mere negativity
Kveraga, K., Boshyan, J., Adams, R. B., Mote, J., Betz, N., Ward, N., Hadjikhani, N. K., Bar, M., & Barrett, L. F. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu007 · Cited by 77
“A view promoted by Sander, Brosch and colleagues (Sander et al., 2003; Brosch et al., 2010) argues that the amygdala, rather than being simply a ‘fear module’, is involved in broader, subjective appraisal of the motivational relevance of a stimulus.”
BackgroundAbnormal amygdala activation profile in pedophilia
Sartorius, A., Ruf, M., Kief, C., Demirakça, T., Bailer, J., Ende, G., Henn, F. A., Meyer‐Lindenberg, A., & Dreßing, H. R. (2008) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-008-0782-2 · Cited by 73
“Considering the amygdala as a relevance detector in emotion processing [13, 38] we expected a significant difference in activation patterns among pedophile sex-offenders (attracted to boys; while viewing boys) compared to normal heterosexual control subjects.”
BackgroundTheoretical Approaches to Emotion and Its Measurement
Coppin, G., & Sander, D. (2016) · Elsevier eBooks · doi:10.1016/b978-0-08-100508-8.00001-1 · Cited by 92
Self-citationMultimodal evaluation of the amygdala’s functional connectivity
Kerestes, R., Chase, H., Phillips, M., Ladouceur, C., & Eickhoff, S. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.12.023 · Cited by 75
“In line with this view, the amygdala's role is to evaluate the behavioral salience and motivational properties of sensory stimuli, as well as to subsequently generate appropriate emotional, autonomic and motor responses through connections with hypothalamic, thalamic and cortical brain regions (Sander et al., 2003).”
BackgroundImpaired threat prioritisation after selective bilateral amygdala lesions
Bach, D. R., Hurlemann, R., & Dolan, R. J. (2014) · Cortex · doi:10.1016/j.cortex.2014.08.017 · Cited by 72
Response and habituation of the amygdala during processing of emotional prosody
Wiethoff, S., Wildgruber, D., Grodd, W., & Ethofer, T. (2009) · Neuroreport · doi:10.1097/wnr.0b013e328330eb83 · Cited by 81
The BOLD signal in the amygdala does not differentiate between dynamic facial expressions
van der Gaag, C., Minderaa, R. B., & Keysers, C. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm002 · Cited by 74
“This view of the amygdala is similar to that put forward by others (Whalen et al., 1998; Holland and Gallagher, 1999; Sander et al., 2003; Adolphs et al., 2005).”
ResultMüller, V. I., Höhner, Y., & Eickhoff, S. B. (2018) · Cortex · doi:10.1016/j.cortex.2018.03.011 · Cited by 73
The influence of emotional stimuli on the oculomotor system: A review of the literature
Mulckhuyse, M. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-0590-8 · Cited by 78
‘Emotional Intelligence’: Lessons from Lesions
Hogeveen, J., Salvi, C., & Grafman, J. H. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.08.007 · Cited by 82
“It has recently been argued that the amygdala plays a role in coordinating the enhanced consolidation and recall of emotionally salient information relative to more affectively neutral contextual information [60], similar to the way it amplifies processing of salient information online during emotion recognition tasks…”
BackgroundSelf-citationNothing to fear? Neural systems supporting avoidance behavior in healthy youths
Schlund, M. W., Siegle, G. J., Ladouceur, C. D., Silk, J. S., Cataldo, M. F., Forbes, E. E., Dahl, R. E., & Ryan, N. D. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.244 · Cited by 74
“…state remains unclear, but the significant increase in activation observed and subsequent avoidance is consistent with the proposal that the amygdala responded to a salient event that derived its aversive motivational properties through prior association with money loss (Sander et al., 2003 ).”
Detection of propensity for aggression based on facial structure irrespective of face race
Short, L. A., Mondloch, C. J., McCormick, C. M., Carré, J. M., Ma, R., Fu, G., & Lee, K. (2011) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2011.07.002 · Cited by 68
“The underlying mechanism likely involves brain structures in the limbic system and the amygdala in particular, which has been implicated in the implicit assessment of various stimuli (Sander et al., 2003) and judgments of social valence such as trustworthiness (Todorov & Engell, 2008; Winston et al.”
BackgroundAffective scenes influence fear perception of individual body expressions
den Stock, J. V., Vandenbulcke, M., Sinke, C. B. A., & de Gelder, B. (2012) · Human Brain Mapping · doi:10.1002/hbm.22195 · Cited by 69
“In fact, there is also accumulating evidence from face-perception studies in normal [Fusar-Poli et al., 2009; Herry et al., 2007; Sander et al., 2003; Santos et al., 2011] and clinical populations [Piech et al., 2011; Terburg et al., 2012], challenging the notion that the amygdala is specifically…”
BackgroundFormal Models of the Network Co-occurrence Underlying Mental Operations
Bzdok, D., Varoquaux, G. P., Grisel, O., Eickenberg, M., Poupon, C., & Thirion, B. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004994 · Cited by 61
“Amygdala activity, in turn, responds reliably to environmental information that carries emotional, social, or motivational value, generally stimuli of evolutionary salience [106].”
BackgroundInfluence of adult attachment style on the perception of social and non-social emotional scenes
Vrtička, P., Sander, D., & Vuilleumier, P. O. (2012) · Journal of Social and Personal Relationships · doi:10.1177/0265407512443451 · Cited by 74
“…in the amygdala (Lemche et al., 2006; Vrticˇka et al., 2008), a region associated with fear and personal relevance (Phelps & LeDoux, 2005; Sander, Grafman, & Zalla, 2003), while conversely, AV correlates with weaker response to positive social stimuli (smiling faces) in the ventral…”
Self-citationAssociated motivational salience impacts early sensory processing of human faces
Hammerschmidt, W., Reulen, H.-J., & Schacht, A. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.04.032 · Cited by 62
“A network of several brain regions suggested to enable a rapid detection of emotionally and motivationally relevant stimuli includes the direct link between sensory pathways and the amygdala (Sander et al., 2003) as well as other subcortical (e.”
de Houwer, J., & Hermans, D. (2010) · Psychology Press eBooks · doi:10.4324/9780203853054 · Cited by 73
Comment: On the Role of Appraisal Processes in the Construction of Emotion
Brosch, T. (2013) · Emotion Review · doi:10.1177/1754073913489752 · Cited by 64
The effect of emotional arousal on visual attentional performance: a systematic review
Zsido, A. N. (2023) · Psychological Research · doi:10.1007/s00426-023-01852-6 · Cited by 90
“Separating this relevance effect from the arousal effect is difficult, although appraisal theories only posit that stimuli appraised affectively relevant have facilitated access to attention (Brosch et al., 2013; Sander et al., 2003).”
BackgroundMishra, A., Rogers, B. P., Chen, L. M., & Gore, J. C. (2013) · Human Brain Mapping · doi:10.1002/hbm.22249 · Cited by 66
“The most established functions are probably the storage of conditioned stimulus–unconditioned stimulus associations in fear conditioning, and its role in relevance detection [Sander et al., 2003].”
BackgroundDistinct Brain Areas involved in Anger versus Punishment during Social Interactions
Klimecki, O., Sander, D., & Vuilleumier, P. O. (2018) · Scientific Reports · doi:10.1038/s41598-018-28863-3 · Cited by 67
“In humans, amygdala activity signals motivational relevance 33,34 , whether for positive or negative events 35,37 , and promotes learning of associations with rewards or punishments 38 .”
Self-citationRymarczyk, K., Żurawski, Ł., Jankowiak-Siuda, K., & Szatkowska, I. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00701 · Cited by 73
Emotion regulation across the life span
Helion, C., Krueger, S. M., & Ochsner, K. N. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-12-804281-6.00014-8 · Cited by 78
“…brain regions involved in triggering an affective response (Ochsner et al., 2009; Lindquist et al., 2012), in large part because it is thought to signal the presence of goal-relevant stimuli, and emotions arise from appraisals of goal relevance (Sander et al., 2003; Cunningham and Brosch, 2012).”
BackgroundBrain Responses to Dynamic Facial Expressions: A Normative Meta-Analysis
Zinchenko, O. O., Yaple, Z. A., & Arsalidou, M. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00227 · Cited by 67
Potential threat attracts attention and interferes with voluntary saccades.
Schmidt, L. J., Belopolsky, A. V., & Theeuwes, J. (2015) · Emotion · doi:10.1037/emo0000041 · Cited by 63
“The amygdala detects and processes information about potentially relevant stimuli and their relationship to an individual's current goals or needs (Sander et al., 2003).”
BackgroundSchiller, D., Yu, A. N. C., Alia‐Klein, N., Becker, S., Cromwell, H. C., Dolcos, F., Eslinger, P. J., Frewen, P., Kemp, A. H., Pace-Schott, E. F., et al. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105450 · Cited by 89
The hyper-sentient addict: an exteroception model of addiction
DeWitt, S. J., Ketcherside, A., McQueeny, T. M., Dunlop, J. P., & Filbey, F. M. (2015) · The American Journal of Drug and Alcohol Abuse · doi:10.3109/00952990.2015.1049701 · Cited by 66
“While exteroception refers to the perception of all external stimuli, the stimuli’s relevance to the self is processed by the Relevance Detector Network (RDN) with the amygdala as its primary node (22).”
Reprint of: Emotion and cognition and the amygdala: From “what is it?” to “what's to be done?”
Pessoa, L. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.02.030 · Cited by 65
Empathy for Pain from Adolescence through Adulthood: An Event-Related Brain Potential Study
Mella, N., Studer, J., Gilet, A.-L., & Labouvie‐Vief, G. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00501 · Cited by 63
“…have for example shown that merely viewing emotional pictures generated enhanced activity of the amygdala in adolescents as compared to adults or young children (Hare et al., 2008); this may be interpreted as a sign of higher relevance of emotional information in adolescence (Sander et al., 2003).”
BackgroundIs the voice an auditory face? An ALE meta-analysis comparing vocal and facial emotion processing
Schirmer, A. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx142 · Cited by 63
“This enhancement occurs most consistently within the amygdala, which presumably serves as a relevance detector (Sander et al., 2003), supports identity processing (Rutishauser et al.”
BackgroundMoors, A. (2017) · Psychological Inquiry · doi:10.1080/1047840x.2017.1235900 · Cited by 70
The Neurobiological Correlates of Gaze Perception in Healthy Individuals and Neurologic Patients
Battaglia, S., Fabius, J. H., Moravkova, K., Fracasso, A., & Borgomaneri, S. (2022) · Biomedicines · doi:10.3390/biomedicines10030627 · Cited by 61
“These findings confirm the amygdala’s role in encoding the perceived threat level of faces, as well as the more general assumption that the amygdala encodes the relevance or significance of a stimulus to the observer [94].”
BackgroundRobust Selectivity for Faces in the Human Amygdala in the Absence of Expressions
Mende‐Siedlecki, P., Verosky, S. C., Turk‐Browne, N. B., & Todorov, A. T. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00469 · Cited by 59
“The present research adds to a growing compendium of evidence reframing the role of the amygdala in social perception (Todorov, 2012; Adolphs, 2010; Cunningham, Van Bavel, & Johnsen, 2008; Sander et al., 2003).”
MethodDiscrete dynamic Bayesian network analysis of fMRI data
Burge, J., Lane, T. D. R., Link, H., Qiu, S., & Clark, V. P. (2007) · Human Brain Mapping · doi:10.1002/hbm.20490 · Cited by 59
“The amygdala is central to the perception and expression of anxiety in humans and other primates [Sander et al., 2003] especially in children [Amaral et al., 2003], with a diminution of its influence with normal aging [Bauman et al., 2004].”
BackgroundRepresentation of perceived sound valence in the human brain
Viinikainen, M., Kätsyri, J., & Sams, M. E. (2011) · Human Brain Mapping · doi:10.1002/hbm.21362 · Cited by 63
“Keywords: emotion; valence; fMRI; amygdala; auditory cortex; prefrontal cortex r r”
Pourtois, G., Spinelli, L., Seeck, M., & Vuilleumier, P. O. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21404 · Cited by 62
The Role of Emotion Regulation in Moral Judgment
Helion, C., & Ochsner, K. N. (2016) · Neuroethics · doi:10.1007/s12152-016-9261-z · Cited by 69
“Amygdala Detecting and responding to affective stimuli [55, 56] Correlated with implicit moral attitude strength [57]”
BackgroundReduced emotion processing efficiency in healthy males relative to females
Weisenbach, S. L., Rapport, L. J., Briceño, E. M., Haase, B. D., Vederman, A. C., Bieliauskas, L. A., Welsh, R. C., Starkman, M. N., McInnis, M. G., Zubieta, J., et al. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss137 · Cited by 60
“Given that the amygdala has been conceptualized as a ‘relevance detector’ (Sander et al., 2003), this finding suggests that for females, negative emotions are most relevant, whereas for males, positive and negative emotions are salient.”
BackgroundSteps to a “Properly Embodied” cognitive science
Stapleton, M. (2012) · Cognitive Systems Research · doi:10.1016/j.cogsys.2012.05.001 · Cited by 61
“This framework resulted in interpreting data in such a way that the amygdala has generally become thought of as a “ rapid-response fear module ” (for a detailed rejection of this view, see Sander, Grafman, & Zalla, 2003).”
BackgroundMethodOmigie, D., Pearce, M. T., Lehongre, K., Hasboun, D., Navarro, V., Adam, C., & Samson, S. (2019) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01388 · Cited by 57
“First, in line with evidence of its involvement in the detection of salient events (Sander et al., 2003), the processing of unexpected musical chords (Koelsch, Fritz, et al., 2008), as well as tension in real music (Lehne et al., 2014), we predicted we would observe sensitivity to IC in the…”
BackgroundImpaired selection of relevant positive information in depression
Levens, S. M., & Gotlib, I. H. (2009) · Depression and Anxiety · doi:10.1002/da.20565 · Cited by 59
“Although the specific neural mechanisms that underlie the selection of relevant positive stimuli in depression have not yet been elucidated, it is likely that the amygdala, because of its involvement in the processing of relevant([35]) and emotional stimuli, and the prefrontal cortex (PFC), which has been shown to reg…”
BackgroundLucas, N., & Vuilleumier, P. O. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.12.027 · Cited by 58
Altruistic behavior: mapping responses in the brain
Filkowski, M. M., Cochran, R. N., & Haas, B. W. (2016) · Neuroscience and Neuroeconomics · doi:10.2147/nan.s87718 · Cited by 64
“58 The insula is involved in processing of emotional stimuli; particularly negative stimuli, in addition to interoceptive states.”
Brosch, T., Coppin, G., Scherer, K. R., Schwartz, S., & Sander, D. (2010) · Social Neuroscience · doi:10.1080/17470919.2010.506754 · Cited by 74
Self-citationSpatial frequencies and emotional perception
Cesarei, A. D., & Codispoti, M. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0053 · Cited by 63
“It has been shown that the relevance of stimuli that can determine an enhanced amygdala response may depend on the novelty, informative value, and motivational significance of both positive and negative emotional stimuli (Sander et al., 2003; Lang and Bradley, 2010; Sabatinelli et al., 2011).”
BackgroundCognitive function, origin, and evolution of musical emotions
PERLOVSKY, L. I. (2012) · Musicae Scientiae · doi:10.1177/1029864912448327 · Cited by 58
The amygdala, top-down effects, and selective attention to features
Jacobs, R. H. A. H., Renken, R. J., Aleman, A., & Cornelissen, F. W. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.05.011 · Cited by 61
Positive emotions have a unique capacity to capture attention
Gupta, R. (2019) · Progress in brain research · doi:10.1016/bs.pbr.2019.02.001 · Cited by 64
Murray, E., Brouwer, S., McCutcheon, R. A., Harmer, C. J., Cowen, P. J., & McCabe, C. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3573-7 · Cited by 55
“They found food reward-related activation attenuated by GSK1521498 only in the amygdala region of interest, a region reported to be involved in both appetitive and aversive processing and salience detection (Morrison and Salzman 2010; Sander et al. 2003).”
BackgroundPinkham, A. E., Loughead, J., Ruparel, K., et al. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.10060832 · Cited by 56
Conty, L., & Grèzes, J. (2011) · Human Brain Mapping · doi:10.1002/hbm.21366 · Cited by 55
“Keywords: direct gaze; emotion; fMRI; hippocampus; memory r r”
BackgroundLateralized interactive social content and valence processing within the human amygdala
Vrtička, P., Sander, D., & Vuilleumier, P. O. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00358 · Cited by 61
“This concept of relevance detection has its origins in emotion psychology (Sander et al., 2003), in particular in appraisal theories of emotion (Sander et al.”
BackgroundResultInfluentialSelf-citationPilarczyk, J., & Kuniecki, M. (2014) · Journal of Vision · doi:10.1167/14.12.4 · Cited by 53
Motivation Matters: Differing Effects of Pre-Goal and Post-Goal Emotions on Attention and Memory
Kaplan, R. L., Damme, I. V., & Levine, L. J. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00404 · Cited by 64
“Goals associated with discrete emotions (e.g., the goal of avoiding threat when fear) may promote processing of goal-relevant information and impair processing of information that is peripheral”
John, Y. J., Zikopoulos, B., Bullock, D. H., & Barbas, H. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004722 · Cited by 58
“Such a role has been proposed as a unifying explanation of a variety of neuroimaging and patient studies of the human amygdala, and as an alternative to the idea that the amygdala serves as a dedicated ‘fear module’ [57].”
BackgroundInfluentialThe development of spontaneous facial responses to others’ emotions in infancy: An EMG study
Kaiser, J., Crespo-Llado, M. M., Turati, C., & Geangu, E. (2017) · Scientific Reports · doi:10.1038/s41598-017-17556-y · Cited by 58
Interaction between a history of depression and rumination on neural response to emotional faces
Thomas, E. J., Elliott, R., McKie, S., Arnone, D., Downey, D., Juhász, G., Deakin, J. F. W., & Anderson, I. M. (2011) · Psychological Medicine · doi:10.1017/s0033291711000043 · Cited by 53
“2002), but not all (Sander et al. 2003 ; Fitzgerald et al. 2006), previous studies have suggested.”
BackgroundMothers' amygdala response to positive or negative infant affect is modulated by personal relevance
Strathearn, L., & Kim, S. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00176 · Cited by 59
“These results are consistent with the view that the amygdala functions as a “relevance detector,” a concept first proposed by Sander et al. (2003).”
BackgroundResultTime Scales of Auditory Habituation in the Amygdala and Cerebral Cortex
Mutschler, I., Wieckhorst, B., Speck, O., Schulze‐Bonhage, A., Hennig, J., Seifritz, E., & Ball, T. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq001 · Cited by 52
“stimuli might reflect the fact that the sensory stimuli are no longer of relevance for the individuals because the amygdala is thought to be essential in evaluating stimulus salience and in initiating behavioral responses (Sander et al. 2003).”
BackgroundMorel‐Kohlmeyer, S., Beaucousin, V., Perrin, M., & George, N. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.04.016 · Cited by 57
“This may appear at odds with the widely accepted idea of a prioritised processing of negative, threat-related stimuli (Adolphs, 2002; Ohman et al., 2001a, 2001b; Sander et al., 2003).”
Elsey, J., Coates, A., Lacadie, C. M., McCrory, E. J., Sinha, R., Mayes, L. C., & Potenza, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.6 · Cited by 52
Trait impulsivity is related to ventral ACC and amygdala activity during primary reward anticipation
Kerr, K. L., Avery, J. A., Barcalow, J. C., Moseman, S. E., Bodurka, J., Bellgowan, P. S. F., & Simmons, W. K. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu023 · Cited by 56
“The amygdala, which in this study also exhibited activity and functional connectivity related to trait impulsivity, supports emotional coding of stimulus value, providing an emotional context, or arousal, that modulates responses to reward cues (Baxter and Murray, 2002; Anderson et al., 2003; Sander et al., 2003; Smal…”
Buechner, V. L., Maier, M., Lichtenfeld, S., & Schwarz, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108111 · Cited by 53
“Emotional human facial stimuli specifically function to non-verbally communicate motive-relevant information to the perceiver (see [80–83] for the goal-relevance of human faces).”
BackgroundApathy following traumatic brain injury: A review
Worthington, A. D., & Wood, R. L. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.04.012 · Cited by 53
“Although associated with fear and rage it may be involved more broadly in detecting stimulus relevance (Sander et al., 2003) disruption of which may lead to failure to recognise events that require a response.”
Derntl, B., Habel, U., Robinson, S., Windischberger, C., Kryspin‐Exner, I., Gur, R. C., & Moser, E. (2009) · Social Neuroscience · doi:10.1080/17470910802571633 · Cited by 54
Moors, A. (2012) · Consciousness & emotion book series · doi:10.1075/ceb.7.13moo · Cited by 50
Amygdala function in emotion, cognition, and behavior
Domínguez‐Borràs, J., & Vuilleumier, P. O. (2022) · Handbook of clinical neurology · doi:10.1016/b978-0-12-823493-8.00015-8 · Cited by 56
Amygdala involvement in self-blame regret
Nicolle, A., Bach, D. R., Frith, C., & Dolan, R. J. (2010) · Social Neuroscience · doi:10.1080/17470919.2010.506128 · Cited by 50
Woolley, J. D., Strobl, E. V., Sturm, V. E., Shany‐Ur, T., Poorzand, P., Grossman, S. N., Nguyen, L. A., Eckart, J. A., LEVENSON, R. W., Seeley, W. W., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.031 · Cited by 53
“The role of the amygdala in emotional signal detection is well established (44,45), and the temporal regions found in our study have been widely associated with both socioemotional (right .”
BackgroundHan, K., Chapman, S. B., & Krawczyk, D. C. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00231 · Cited by 56
Moriguchi, Y., Negreira, A. M., Weierich, M. R., Dautoff, R. J., Dickerson, B. C., Wright, C. I., & Barrett, L. F. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21527 · Cited by 51
The maternal brain: Neural responses to infants in mothers with and without mood disorder
Bjertrup, A. J., Friis, N. K., & Miskowiak, K. W. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.011 · Cited by 50
Rapid Stress System Drives Chemical Transfer of Fear from Sender to Receiver
de Groot, J. H. B., Smeets, M. A. M., & Semin, G. R. (2015) · PLOS ONE · doi:10.1371/journal.pone.0118211 · Cited by 50
“The amygdala was argued to be neither a fear module, nor a negative-emotions-dedicated subsystem, but rather a relevance detector [81].”
BackgroundDeep brain stimulation for severe autism: from pathophysiology to procedure
Sinha, S. R., McGovern, R. A., & Sheth, S. A. (2015) · Neurosurgical FOCUS · doi:10.3171/2015.3.focus1548 · Cited by 52
Brain activation during direct and indirect processing of positive and negative words
Straube, T., Sauer, A., & Miltner, W. H. R. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.037 · Cited by 56
Altered amygdala-prefrontal connectivity during emotion perception in schizophrenia
Bjorkquist, O. A., Olsen, E., Nelson, B. D., & Herbener, E. S. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.04.003 · Cited by 51
What can vigilance tell us about fear?
Beauchamp, G. (2017) · Animal Sentience · doi:10.51291/2377-7478.1203 · Cited by 50
Metadata
- 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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