Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): Generality and individual consistency of effects.

Mason, William A.; Capitanio, John P.; Machado, Christopher J.; Mendoza, Sally P.; Amaral, David G.

doi:10.1037/1528-3542.6.1.73

Cited by 92 publications

(129 citation statements)

References 22 publications

(56 reference statements)

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“…Intriguingly, recent theories of amygdala function argue that the amygdala subserves an abstract function in detecting uncertainty (13) or ambiguity (14) in the environment and in triggering arousal and vigilance as a consequence. This hypothesis is consistent with a tendency for amygdalalesioned monkeys to approach stimuli that healthy monkeys avoid (15), as well as greater amygdala activation in people with more inhibited personalities (16). Furthermore, a recent study found that increased cognitive control of the autonomic emotional responses normally elicited by losses significantly reduced the susceptibility to loss aversion (17).…”

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confidence: 76%

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Amygdala damage eliminates monetary loss aversion

Martino

Camerer

Adolphs

2010

Proc. Natl. Acad. Sci. U.S.A.

368

301

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Losses are a possibility in many risky decisions, and organisms have evolved mechanisms to evaluate and avoid them. Laboratory and field evidence suggests that people often avoid risks with losses even when they might earn a substantially larger gain, a behavioral preference termed "loss aversion." The cautionary brake on behavior known to rely on the amygdala is a plausible candidate mechanism for loss aversion, yet evidence for this idea has so far not been found. We studied two rare individuals with focal bilateral amygdala lesions using a series of experimental economics tasks. To measure individual sensitivity to financial losses we asked participants to play a variety of monetary gambles with possible gains and losses. Although both participants retained a normal ability to respond to changes in the gambles' expected value and risk, they showed a dramatic reduction in loss aversion compared to matched controls. The findings suggest that the amygdala plays a key role in generating loss aversion by inhibiting actions with potentially deleterious outcomes.oss aversion describes the widespread behavioral avoidance of choices that can lead to losses, even when accompanied by equal or much larger gains. This phenomenon was first proposed as part of "prospect theory" (1), a theory of choice among monetary gambles. Across many studies, losses typically loom about 1.5-2 times as large as gains: for instance, people will avoid gambles in which they are equally likely to either lose $10 or win $15, even though the expected value of the gamble is positive ($2.50). Loss aversion has been well documented in the laboratory and in many field settings (2), including high-stakes game show decisions (3), financial markets (4), politics (5), trade policy for declining industries (6), rate of organ donation for transplant cases (7) and has also been evident in monkey behavior (8). But what drives loss-averse behavior, and what neural structures mediate the effect?Our study tested the hypothesis that the amygdala mediates loss aversion, an idea motivated by a large literature implicating this brain structure in processing fear and threat (9), as well as in anticipation and experience of monetary loss (10). Given the amygdala's prominent role in affective processing, it is also relevant to note that loss aversion appears to increase with affective enrichment of "hedonic" consumer goods (e.g., music CDs versus computer disks) (11) and more generally with emotional attachment (12). Intriguingly, recent theories of amygdala function argue that the amygdala subserves an abstract function in detecting uncertainty (13) or ambiguity (14) in the environment and in triggering arousal and vigilance as a consequence. This hypothesis is consistent with a tendency for amygdalalesioned monkeys to approach stimuli that healthy monkeys avoid (15), as well as greater amygdala activation in people with more inhibited personalities (16). Furthermore, a recent study found that increased cognitive control of the autonomic emotional responses normall...

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supporting

confidence: 76%

“…even though they will approach foods that are paired with potentially threatening stimuli more quickly than control monkeys (15).…”

Section: Discussionmentioning

confidence: 99%

Amygdala damage eliminates monetary loss aversion

Martino

Camerer

Adolphs

2010

Proc. Natl. Acad. Sci. U.S.A.

368

301

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“…We believe this evidence suggests that heightened affiliative social interactions following amygdala lesions stems from a more general inability to properly perceive danger or threat in the environment and use such information to modulate social behavior adaptively. In line with this view, deficits in threat detection or fear reactivity have been specifically demonstrated for monkeys with bilateral neurotoxic amygdala lesions in both social (Machado & Bachevalier, 2006) and nonsocial settings (Izquierdo, Suda, & Murray, 2005;Kalin, Shelton, & Davidson, 2004;Kalin, Shelton, Davidson, & Kelley, 2001;Mason et al, 2006;Meunier, Bachevalier, Murray, Málková, & Mishkin, 1999). These abnormalities are not restricted to nonhuman primates, since humans with amygdala lesions also demonstrate specific deficits in identifying fearful facial expressions (Adolphs et al, 1999), rating the magnitude of fearful expressions (Adolphs, Tranel, Damasio, & Damasio, 1995) and assessing the approachability or trustworthiness of unfamiliar individuals (Adolphs, Tranel, & Damasio, 1998).…”

Section: Social Disinhibition Persists Across Contextsmentioning

confidence: 80%

Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts.

Machado

Emery

Capitanio

et al. 2008

Behavioral Neuroscience

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Although the amygdala has been repeatedly implicated in normal primate social behavior, great variability exists in the specific social and nonsocial behavioral changes observed after bilateral amygdala lesions in nonhuman primates. One plausible explanation pertains to differences in social context. To investigate this idea, we measured the social behavior of amygdala-lesioned and unoperated rhesus monkeys (Macaca mulatta) in two contexts. Animals interacted in four-member social groups over 32 test days. These animals were previously assessed in pairs (Emery et al., 2001), and were, therefore, familiar with each other at the beginning of this study. Across the two contexts, amygdala lesions produced a highly consistent pattern of social behavior. Operated animals engaged in more affiliative social interactions with control group partners than did control animals. In the course of their interactions, amygdala-lesioned animals also displayed an earlier decrease in nervous and fearful personality qualities than controls. The increased exploration and sexual behavior recorded for amygdala-lesioned animals in pairs was not found in the four-member groups. We conclude that the amygdala contributes to social inhibition and this function transcends various social contexts.

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“…Alternatively, the amygdala could contribute to behaviours that support social hierarchy, including gaze-following [88] and theory of mind (ToM) [89] (see below). The amygdala could also contribute to social rank via interpersonal behaviours or personality traits, such as aggression [90], grooming [90] or fear responses [91,92]. Finally, scaling of the activity of neurons in parietal cortex, and possibly other areas, by the rank of other individuals in the visible scene [76] likely mediates the selective allocation of attention to dominant individuals over subordinates in many primate groups [1,13,93] Together, these studies, and others like them, suggest the following back-of-the-envelope framework for the organization of basic social processes in the primate brain.…”

Section: Mechanisms Mediating the Evaluation Of Social Partners' Valumentioning

confidence: 99%

Adaptations for social cognition in the primate brain

Platt

Seyfarth

Cheney

2016

Phil. Trans. R. Soc. B

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One contribution of 18 to a theme issue 'The evolution of cooperation based on direct fitness benefits'. Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals' fitness interdependent and the 'free-rider' problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation-often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and nonsocial decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and nonhuman primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.

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Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): Generality and individual consistency of effects.

Cited by 92 publications

References 22 publications

Amygdala damage eliminates monetary loss aversion

Amygdala damage eliminates monetary loss aversion

Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts.

Adaptations for social cognition in the primate brain

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