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The Amygdala, Social Behavior, and Danger Detection
Open accessAbstract
The amygdala is a distinctive portion of the anterior temporal lobe that has been implicated in a variety of functions including expression of fear, modulation of memory, and mediation of social communication. While work on the rodent amygdala often deals with emotion, much of the research in nonhuman primates and in man deals with its role in the perception of social signals, such as facial expressions, and the maintenance of social position, such as in primate dominance hierarchies. We have established a program of research that has as its major goal the definition of neural systems that underlie species-typical social communication. A first phase of the program was launched on the premise that the amygdala is essential for species-typical social behavior. We sought to examine in more detail the impairments of social behavior that followed discrete, bilateral lesions of the amygdala. We found, however, that mature rhesus monkeys with bilateral lesions of the amygdala not only were capable of species-typical social behavior, but actually engaged in more affiliative social interactions. The lesioned animals also demonstrated a striking lack of fear of normally fear-inducing stimuli such as replicas of snakes. In a second, ongoing series of studies in the infant rhesus monkey, we are examining whether the amygdala is essential for gaining social knowledge during development. Infant animals that receive bilateral lesions of the amygdala at two weeks of age and are raised by their biological mothers demonstrate all expected social behaviors for their ages. These animals, like the adults, demonstrate a lack of fear of objects such as snakes. However, unlike the adults, they demonstrate more fear when placed into novel social situations. The results from these studies are most consistent with the conclusion that the amygdala is not necessary for species-typical social behavior or for gaining social knowledge during development. We hypothesize that the amygdala is a critical component of a system that evaluates the environment for potential dangers. As such, it has a modulatory role on social behavior-that is, it typically inhibits social interaction with novel conspecifics while they are evaluated as potential adversaries. This perspective predicts that hyperactivity of the amygdala would be associated with increased fear or anxiety and may contribute to disorders such as social phobia.
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“In particular, trauma experienced from a caregiver during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species (Amaral, 2003, Callaghan et al., 2014, McEwen, 2003, Moriceau et al., 2006, Tang et al., 2014, Tzanoulinou and Sandi, 2017, Zeanah et al., 2003).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Amaral, 2003
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“Across many species, many of the effects of infant abuse remain latent until peri-adolescence (Adriani and Laviola, 2004, Amaral, 2003, Andersen and Teicher, 2008, Bauman et al., 2006, Costello et al., 2003).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Amaral, 2003
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“The most dramatic developmental differences were first observed in non-human primates, where infant amygdala lesions lead to decreased fear response to normally threatening stimuli and an enhanced response to novel social situations (Amaral, 2002, Amaral, 2003).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Amaral, 2003
In the citing paper
“Moreover, studies in nonhuman primates demonstrate that adult monkeys without amygdalae display inappropriate social behavior (Amaral, 2003, Baron-Cohen et al., 2000, Bliss-Moreau et al., 2011, Brothers et al., 1990, Emery et al., 2001, Malkova et al., 2010).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Amaral, 2003
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Citations
Cites
The amygdala: vigilance and emotion
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The human amygdala in social judgment
Adolphs, R., Tranel, D., & Damasio, A. R. (1998) · Nature · doi:10.1038/30982 · Cited by 1,125
The Human Amygdala in Social Judgment
Adolphs, R., Tranel, D., & Damásio, A. R. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0027 · Cited by 881
Recognition of facial emotion in nine individuals with bilateral amygdala damage
Adolphs, R., Tranel, D., Hamann, S. B., Young, A. W., Calder, A. J., Phelps, E. A., Anderson, A. K., Lee, G. P., & Damásio, A. R. (1999) · Neuropsychologia · doi:10.1016/s0028-3932(99)00039-1 · Cited by 778
Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys
Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., & Insel, T. R. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300128 · Cited by 345
Influence of amygdalectomy on social behavior in monkeys.
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Research works printed but not linked: 1
- Kling A.S. & L.A. Brothers. 1992. The amygdala and social behavior.InThe Amygdala: Neurobiological Aspects of Emotion Memory and Mental Dysfunction: 353–377. Wiley‐Liss. New York.
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Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203
“Further, it is consistent with the results of the primate mentioned studies above suggesting a role for the amygdala in social emotions (Amaral, 2003).”
BackgroundResultOxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans
Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., Gruppe, H., Mattay, V. S., Gallhofer, B., & Meyer-Lindenberg, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-05.2005 · Cited by 1,639
“nal in social interaction (Amaral, 2003), both conscious and im-”
BackgroundResultRethinking the Emotional Brain
LeDoux, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.004 · Cited by 1,594
“…survival functions such as defense (e.g., LeDoux, 1996, 2012; Phelps and LeDoux, 2005; Motta et al., 2009; Choi et al., 2005; Kalin et al., 2004; Amaral, 2003; Antoniadis et al., 2007), reproduction (e.g., Pfaff, 1999; Oomura et al., 1988; Blaustein, 2008), thermoregulation (Nakamura and…”
Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.009 · Cited by 1,258
“A vast area of research in animal, human lesion, and neuroimaging studies points to the critical role of these brain areas in signaling and modulating fear responses (Adolphs et al., 2005; Amaral, 2003).”
Advancing the understanding of autism disease mechanisms through genetics
de la Torre-Ubieta, L., Won, H., Stein, J. L., & Geschwind, D. H. (2016) · Nature Medicine · doi:10.1038/nm.4071 · Cited by 827
“The amygdala is another candidate region that may be affected in ASD because of its role in modulating fear and social behavior 202,207,208 .”
Metadata
- Authors
- AMARAL, D. G.
- Affiliations
- University of California, Davis (US)
- Corresponding author
- AMARAL, DAVID G.
- ORCID
- AMARAL, DAVID G.
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 2003-12
- Volume
- 1000
- Issue
- 1
- Pages
- 337-347
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W1964983039
- Cited by
- 293
- References
- 33
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 15 · 2020: 8 · 2019: 10 · 2018: 9 · 2017: 20 · 2016: 18 · 2015: 12 · 2014: 14 · 2013: 19 · 2012: 20
- FWCI
- 5.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- amygdala, social behavior, threat detection, rhesus monkeys, infant rhesus monkeys, fear of snakes, social communication, affiliative behavior, dominance hierarchy, social anxiety disorder, anxiety
- MeSH terms
- Affect, Amygdala, Animals, Anxiety, Fear, Humans, Macaca mulatta, Social Behavior, Social Perception, Temporal Lobe, Signal Detection, Psychological
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