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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Trauma experienced from an attachment figure during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species.
“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
Across many species, many effects of infant abuse remain latent until peri-adolescence.
“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
In non-human primates, infant amygdala lesions lead to decreased fear response to normally threatening stimuli and enhanced response to novel social situations.
“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
Adult monkeys without amygdalae display inappropriate social behavior.
“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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“Relevant for the present context, via the thalamus the amygdala receives input not only from the visual modality but from all senses (Nishijo et al., 1988; Amaral et al., 1992; Amaral, 2003).”
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“But a direct relationship between amygdaloid lesions and reduced fear need not always be the case as the amygdala has been implicated in other functions as well, such as memory (Amaral, 2003; McGaugh et al., 1996) and olfaction (Buck, 1996).”
BackgroundNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157 · see citing works
“Neurons in BLA appear to categorize social events as similar as long as there is a live agent involved (Self, Other, or Both), and do so only during active decision-making, with all its attendant motivational, emotional, and attentional components (17, 21, 24, 56, 57).”
Mackiewicz, K. L., Sarinopoulos, I., Cleven, K. L., & Nitschke, J. B. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601648103 · Cited by 147 · see citing works
Andrewes, D., & Jenkins, L. (2019) · Neuropsychology Review · doi:10.1007/s11065-019-09398-4 · Cited by 138 · see citing works
Novelty as a dimension in the affective brain
Weierich, M. R., Wright, C. I., Negreira, A. M., Dickerson, B. C., & Barrett, L. F. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.047 · Cited by 144 · see citing works
“Several human neuroimaging studies support the idea that amygdala activation is related to the salience or potential information value of visual stimuli (Amaral, 2003; Liberzon, et al., 2003; Whalen et al., 2004), and amygdala engagement has been associated with enhanced memory (e.”
BackgroundInfluentialAmygdala damage affects event‐related potentials for fearful faces at specific time windows
Rotshtein, P., Richardson, M. P., Winston, J. S., Kiebel, S. J., Vuilleumier, P. O., Martin Eimer, A., Driver, J., & Dolan, R. J. (2009) · Human Brain Mapping · doi:10.1002/hbm.20921 · Cited by 179 · see citing works
“Such a positive bias effect has also been observed in monkeys after amygdala damage [Amaral, 2003].”
BackgroundResultFlinn, M. V., Nepomnaschy, P. A., Muehlenbein, M. P., & Ponzi, D. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.01.005 · Cited by 139 · see citing works
The visual analysis of emotional actions
Chouchourelou, A., Matsuka, T., Harber, K. D., & Shiffrar, M. (2006) · Social Neuroscience · doi:10.1080/17470910600630599 · Cited by 138 · see citing works
“For example, rhesus monkeys sustaining bilateral amygdaloid lesions do not react appropriately to potentially dangerous social situations (Amaral, 2003).”
BackgroundResultHadj‐Bouziane, F., Liu, N., Bell, A. H., Gothard, K. M., Luh, W., Tootell, R. B. H., Murray, E. A., & Ungerleider, L. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218406109 · Cited by 132 · see citing works
Pointing with the eyes: The role of gaze in communicating danger
Hadjikhani, N. K., Hoge, R. D., Snyder, J., & de Gelder, B. (2008) · Brain and Cognition · doi:10.1016/j.bandc.2008.01.008 · Cited by 134 · see citing works
“The amygdala is a brain structure essential to the perception of fear (Amaral, 2003; LeDoux, 2003), and activation in the amygdala is reliably produced by presentation of biologically relevant sensory stimuli, and stimuli that predict threat (Whalen, 1998).”
BackgroundAmygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation
Sabatini, M. J., Ebert, P., Lewis, D. A., Levitt, P., Cameron, J. L., & Mirnics, K. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4765-06.2007 · Cited by 125 · see citing works
“In primates, a clear role for the amygdala in social, anxious, and depressive behaviors has been established (Brothers, 1990; Drevets, 1999; Baron-Cohen et al., 2000; Emery et al., 2001; Drevets et al., 2002; Amaral, 2003; Bauman et al., 2004; Etkin et al., 2004; Lorberbaum et al., 2004).”
BackgroundEwbank, M., Lawrence, A. D., Passamonti, L., Keane, J., Peers, P. V., & Calder, A. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.09.056 · Cited by 127 · see citing works
“Human and comparative studies have identified the amygdala as a central component in processing threat-related stimuli (Amaral, 2003; Davis and Whalen, 2001; LeDoux, 2000), playing a predominant role in fear conditioning (LaBar et al., 1995) and processing facial and vocal signals of fear (Adolphs…”
BackgroundGao, W., Salzwedel, A., Carlson, A. L., Xia, K., Azcárate-Peril, M. A., Styner, M. A., Thompson, A. L., Geng, X., Goldman, B. D., Gilmore, J. H., et al. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5161-8 · Cited by 127 · see citing works
“In considering what neural circuits might mediate associations between the gut microbiota and these outcomes, the amygdala has attracted considerable research attention due to its central role in fear (Amaral 2003; Canteras et al. 2010), stress (Ressler 2010), emotional regulation (Banks et al.”
Harper, R. M., Macey, P. M., Woo, M. A., Macey, K. E., Keens, T. G., Gozal, D., & Alger, J. R. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00863.2004 · Cited by 116 · see citing works
The development and neural bases of facial emotion recognition.
Leppänen, J., & Nelson, C. (2006) · Advances in Child Development and Behavior · doi:10.1016/s0065-2407(06)80008-x · Cited by 100 · see citing works
Hypervigilance for fear after basolateral amygdala damage in humans
Terburg, D., Morgan, B. E., Montoya, E. R., Hooge, I. T. C., Thornton, H. B., Hariri, A. R., Panksepp, J., Stein, D. J., & van Honk, J. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.46 · Cited by 110 · see citing works
“therefore argued to be involved in the automatic assessment of threat,(16) and acquisition and extinction of conditioned fear.(6,17,18) Furthermore, the BLA can through mutual connections with the PFC, especially the orbitofrontal cortex (OFC),”
BackgroundImpact of prosocial neuropeptides on human brain function
MEYERLINDENBERG, A. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00436-6 · Cited by 109 · see citing works
“Consistent with the assumption that amygdala activation represents a danger signal in social interaction (Amaral, 2003), both conscious and implicit distrust of faces predicts amygdala activation (Winston et al.”
BackgroundResultInfluentialRoseboom, P. H., Nanda, S. A., Bakshi, V. P., Trentani, A., Newman, S. M., & Kalin, N. H. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.10.002 · Cited by 109 · see citing works
“…the amygdala mediates adaptive and maladaptive fear and anxiety responses (Blanchard and Blanchard, 1972;LeDoux, 2000; Davis and Whalen, 2001; Amaral, 2003; Kalin et al., 2004), it is of particular importance that ferret exposure increased c-fos expression within various nuclei of the…”
BackgroundInfluentialMacey, P. M., Woo, M. A., Macey, K. E., Keens, T. G., Saeed, M. M., Alger, J. R., & Harper, R. M. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00969.2004 · Cited by 110 · see citing works
“A: axial, sagittal, and coronal views of significant response differences between CCHS and control groups in a cluster extending from the right putamen (1) to the claustrum (2) and the ventral insula (3).”
BackgroundInfluentialInteraction between value and perceptual salience in value-driven attentional capture
Wang, L., Yu, H., & Zhou, X. (2013) · Journal of Vision · doi:10.1167/13.3.5 · Cited by 106 · see citing works
“Pain and fear can signal immediate challenge to survival and warn the organism to prepare for the worst (Amaral, 2006; Rogan, Leon, Perez, & Kandel, 2005).”
BackgroundSocial interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice
Stilling, R. M., Moloney, G. M., Ryan, F. J., Hoban, A. E., Bastiaanssen, T. F., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F. (2018) · eLife · doi:10.7554/elife.33070 · Cited by 106 · see citing works
“…and memory, it is also a well-established key emotional brain centre for evaluating and responding to social stimuli in humans and other mammals (Allsop et al., 2014; Amaral, 2003; Kliemann et al., 2012; Noonan et al., 2014; Phelps and LeDoux, 2005; Sabatini et al., 2007; Sallet et al., 2011).”
BackgroundMultiple memory systems: The power of interactions
McDonald, R. J., Devan, B. D., & Hong, N. S. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.05.009 · Cited by 105 · see citing works
“Many researchers have concluded that anxiety disorders must be linked with changes in the hippocampus and/or amygdala (Amaral, 2003; Hariri et al., 2002; Ledoux & Muller, 1997; Quirk & Gehlert, 2003; Walker, Toufexis, & Davis, 2003), and it is possible that these changes occur because of some interaction between the G…”
Burghardt, N. S., & Bauer, E. P. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.050 · Cited by 101 · see citing works
Personality influences the neural responses to viewing facial expressions of emotion
Calder, A. J., Ewbank, M., & Passamonti, L. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0362 · Cited by 98 · see citing works
The development of emotional face and eye gaze processing
Hoehl, S., & Striano, T. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2009.00944.x · Cited by 97 · see citing works
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“…that panic attacks have a non-associative mode of acquisition, and are most probably triggered by impaired orbitofrontal or mediofrontal governance over innate hardwired danger-detection circuits linking the locus ceruleus to the amygdala (Kent et al., 2005; Gorman, 2004; Amaral, 2003).”
Backgroundvan Goozen, S. H. M., & Fairchild, G. F. (2008) · Development and Psychopathology · doi:10.1017/s095457940800045x · Cited by 94 · see citing works
Opendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
“A role for the amygdala in this process is further supported by data in non-human primates showing impaired responses to fearful stimuli following infant amygdala lesions (Amaral, 2003; Bauman et al., 2006; Marquez et al., 2013).”
InfluentialSripada, C., Angstadt, M., Kessler, D. A., Phan, K. L., Liberzon, I., Evans, G. W., Welsh, R. C., Kim, P., & Swain, J. E. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.11.006 · Cited by 93 · see citing works
“The amygdala has been implicated in threat processing (Amaral, 2003; LeDoux, 1998) and in assigning salience to stimuli more broadly (Liberzon et al.”
BackgroundRegional brain responses to pleasant and unpleasant IAPS pictures: different networks.
Aldhafeeri, F. M., Mackenzie, I., Kay, T., Alghamdi, J., & Sluming, V. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.01.064 · Cited by 96 · see citing works
Entis, J. J., Doerga, P. N., Barrett, L. F., & Dickerson, B. C. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.073 · Cited by 88 · see citing works
“…affect (e.g. Adolphs et al., 1994; Barrett et al., 2007; Lanteaume et al., 2007; LeDoux et al., 1988; Sharot et al., 2007), social behavior (e.g. Amaral, 2003; Machado et al., 2008; Rosvold et al., 1954), attention (e.g. Pessoa et al., 2002a, 2002b; Ursin and Kaada, 1960), perception (e.g.…”
Frankó, E., Insausti, A. M., Artacho-Pérula, E., Insausti, R., & Chavoix, C. (2014) · Human Brain Mapping · doi:10.1002/hbm.22170 · Cited by 85 · see citing works
“, 1992], and the amygdala in fear conditioning [Ohman and Mineka, 2001], motivation [Rolls, 1992], social behavior [Adolphs 2010; Amaral, 2003; Meunier and Bechevalier, 2002], and in a wide variety of tasks with an emotional component [Aggleton, 1992; Aggleton, 2000; Gallagher and Chiba, 1996].”
BackgroundInfluentialWeir, R. K., Bauman, M. D., Jacobs, B., & Schumann, C. M. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24332 · Cited by 83 · see citing works
“The amygdala functions as a danger and salience detector and, in turn, plays a key role in social and emotional regulation (Amaral, 2003; Adolphs, 2010).”
BackgroundPrimitive mechanisms of trauma response: an evolutionary perspective on trauma-related disorders.
Baldwin, D. V. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.06.004 · Cited by 85 · see citing works
Neuroanatomic deficits in congenital central hypoventilation syndrome
Kumar, R., Macey, P. M., Woo, M. A., Alger, J. R., Keens, T. G., & Harper, R. M. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20565 · Cited by 85 · see citing works
“…of the cingulate cortex with other limbic sites, including the insula and amygdala, structures which also respond to loaded breathing tasks inducing dyspnea (Banzett et al., 2000; Evans et al., 2002), and, especially in the case of the amygdala, mediate negative emotions (Amaral, 2003).”
BackgroundThe amygdala and FFA track both social and non-social face dimensions
Said, C. P., Dotsch, R., & Todorov, A. T. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.08.009 · Cited by 83 · see citing works
Social Origins of Developmental Risk for Mental and Physical Illness
Cameron, J. L., Eagleson, K. L., Fox, N. A., Hensch, T. K., & Levitt, P. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1822-17.2017 · Cited by 81 · see citing works
“This structure is established as having a clear role in social, anxious, and depressive behaviors in the nonhuman primate (Baron-Cohen et al., 2000; Emery et al., 2001; Drevets et al., 2002; Amaral, 2003; Bauman et al., 2004; Etkin et al., 2004; Lorberbaum et al., 2004).”
BackgroundDoenni, V. M., Gray, J. M., Song, C. M., Patel, S., Hill, M. N., & Pittman, Q. J. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.07.152 · Cited by 80 · see citing works
“Amygdala lesions have been shown to specifically increase social interactions with nonfamiliar animals (shown in primates by Amaral (2003)).”
Kuhlmann, A., Bertsch, K., Schmidinger, I., Thomann, P. A., & Herpertz, S. C. (2013) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.120039 · Cited by 78 · see citing works
Behavioral Inhibition: Temperament or Prodrome?
Pérez‐Edgar, K. E., & Guyer, A. E. (2014) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-014-0019-9 · Cited by 78 · see citing works
Raineki, C., Opendak, M. M., Sarro, E. C., Showler, A., Bui, K., McEwen, B. S., Wilson, D. A., & Sullivan, R. M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907170116 · Cited by 76 · see citing works
“This is consistent with the nonhuman primate literature, where precocious activation of the amygdala puts a brake on social behavior (36, 52, 53).”
BackgroundResultTrevarthen, C., Aitken, K. J., Vandekerckhove, M. M. P., Delafield‐Butt, J. T., & Nagy, E. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch2 · Cited by 78 · see citing works
Pouga, L., Berthoz, S., de Gelder, B., & Grèzes, J. (2010) · Human Brain Mapping · doi:10.1002/hbm.20953 · Cited by 72 · see citing works
Amygdala structure and the tendency to regard the social system as legitimate and desirable
Nam, H. H., Jost, J. T., Kaggen, L., Campbell-Meiklejohn, D. K., & Bavel, J. J. V. (2017) · Nature Human Behaviour · doi:10.1038/s41562-017-0248-5 · Cited by 71 · see citing works
Paying Attention to Social Meaning: An fMRI Study
Tavares, P., Lawrence, A. D., & Barnard, P. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm212 · Cited by 81 · see citing works
Antoniadis, E. A., Winslow, J., Davis, M., & Amaral, D. G. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.07.007 · Cited by 65 · see citing works
Mutual gaze in Alzheimer's disease, frontotemporal and semantic dementia couples
Sturm, V. E., McCarthy, M. E., Yun, I., Madan, A., Yuan, J. W., Holley, S. R., Ascher, E. A., Boxer, A. L., Miller, B. L., & LEVENSON, R. W. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq055 · Cited by 62 · see citing works
“SD patients may be less aware of and less sensitive to negative affect in others because of comprehension difficulties and degeneration of brain structures such as the amygdala, which are important for social behaviors and threat-perception (Aggleton and Passingham, 1981; Amaral, 2003).”
BackgroundKamali, A., Sair, H. I., Blitz, A. M., Riascos, R., Mirbagheri, S., Keser, Z., & Hasan, K. M. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1119-3 · Cited by 61 · see citing works
“…temporal lobe of the brain (Saygin et al. 2011) and is known to have a primary role in processing memory, emotional learning (Davis 1994), decision making (Cohen et al. 2008), social interaction, awareness and fear (Amaral 2003), aggression and sexual behavior (Stoddard-Apter and MacDonnell 1980).”
BackgroundNeural correlates of novelty and face–age effects in young and elderly adults
Wright, C. I., Negreira, A. M., Gold, A. L., Britton, J. C., Williams, D. M., & Barrett, L. F. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.015 · Cited by 61 · see citing works
“…affective processing, it also performs the more basic function of maintaining vigilance (Whalen, 2007) by directing an organism to learn more about a stimulus so as to better determine its predictive value for well-being or survival (Barrett et al., 2007; Rolls, 2005; Whalen, 1998; Amaral, 2003).”
BackgroundZelinski, E. L., Hong, N. S., Tyndall, A. V., Halsall, B., & McDonald, R. J. (2010) · Experimental Brain Research · doi:10.1007/s00221-010-2228-0 · Cited by 61 · see citing works
“This inability is thought to underlie generalized anxiety disorder (GAD) (Mennin et al. 2005), characterized by inappropriately high stress responses relative to a situation or event ( Amaral 2003 ).”
BackgroundGur, R., Ragland, J., Reivich, M., Greenberg, J., Alavi, A., & Gur, R. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn087 · Cited by 57 · see citing works
“The first consisted of resting baseline measures of CMRgl assessed with the F-FDG (F-labeled 2-fluoro2-deoxy-D-glucose) method and published in Gur et al. (1995). That sample included 60 healthy volunteers (37 men, 23 women), age ± SD 27.”
MethodAltinay, M. I., Karne, H. S., & Anand, A. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.06.047 · Cited by 58 · see citing works
“The importance of amygdala in generating emotional responses was shown in numerous studies (Adolphs et al., 2002; Amaral, 2003; Davis, 1992a; Davis and Myers, 2002; Hilton SM, 1963; Kaada, 1972; Kapp BS, 1992; LeDoux, 1992; Sanders and Shekhar, 1995).”
BackgroundHippocampus lesions induced deficits in social and spatial recognition in Octodon degus
Uekita, T., & Okanoya, K. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.01.042 · Cited by 57 · see citing works
What can we learn about emotion by studying psychopathy?
Marsh, A. A. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00181 · Cited by 57 · see citing works
“In addition, most brain lesions occur in late adolescence or adulthood, precluding an understanding of the developmental consequences of lesions to structures like the amygdala, damage to which may result in distinct behavioral outcomes in adulthood relative to infancy (Amaral, 2003).”
BackgroundKlumpp, H., Angstadt, M., Nathan, P. J., & Phan, K. L. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2010.05.001 · Cited by 56 · see citing works
“The amygdala is particularly sensitive to threatening social signals (Zald, 2003), and is critically involved in the perception of potential of danger (Amaral, 2003).”
BackgroundRole of amygdala in drug memory
Luo, Y., Xue, Y.-X., Shen, H., & Lü, L. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.017 · Cited by 55 · see citing works
“Complicated bidirectional projections also exist between higher sensory areas and single sensory areas and the amygdala (Amaral, 2003).”
BackgroundPredator Stress Induces Behavioral Inhibition and Amygdala Somatostatin Receptor 2 Gene Expression
Nanda, S. A., Qi, C., Roseboom, P. H., & Kalin, N. H. (2008) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2008.00401.x · Cited by 55 · see citing works
“Numerous studies suggest that the amygdala mediates both conditioned and unconditioned fear responses (Amaral 2003; Blanchard & Blanchard 1972; Kalin et al. 2004; LeDoux 2000) and human functional imaging studies show that some patients with anxiety and depressive disorders have increased amygdala activation (Drevets…”
BackgroundA “rosy view” of the past: Positive memory biases
Adler, O., & Pansky, A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816660-4.00007-6 · Cited by 52 · see citing works
“Indeed, as one of the most extensively connected subcortical regions of the brain, with links to numerous cortical and subcortical regions (Amaral, 2003; Amaral, Price, Pitkanen, & Carmichael, 1992; LeDoux, 2000), the amygdala has a significant role in all the stages of memory.”
BackgroundAmygdala activation when one is the target of deceit: Did he lie to you or to someone else?
Grèzes, J., Berthoz, S., & Passingham, R. E. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.038 · Cited by 51 · see citing works
“Amaral (2003) has pointed out that the projections of amygdala to visual cortical areas have a typical pattern of feedback-type projections which appear to modulate information processing by enhancing neural responses (Hupe et al., 2001).”
BackgroundVargas-Martínez, F., Uvnás-Moberg, K., Petersson, M., Olausson, H., & Jiménez-Estrada, I. (2014) · Progress in neurobiology · doi:10.1016/j.pneurobio.2014.10.001 · Cited by 49 · see citing works
Dimov, L. F., Toniolo, E. F., Matielo, H. A., de Andrade, D. C., Garcı́a-Larrea, L., Ballester, G., Teixeira, M. J., & Dale, C. S. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.11.036 · Cited by 51 · see citing works
Temporal dynamics of amygdala response to emotion- and action-relevance
Guex, R., Méndez‐Bértolo, C., Moratti, S., Strange, B. A., Spinelli, L., Murray, R. J., Sander, D., Seeck, M., Vuilleumier, P. O., & Domínguez‐Borràs, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-67862-1 · Cited by 50 · see citing works
- 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
- Social Sciences › Psychology › Social Psychology › 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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