The amygdala: is it an essential component of the neural network for social cognition?

Abstract

Observations from human subjects with focal brain lesions and animal subjects with experimental lesions have implicated a variety of brain regions in the mediation of social behavior. Previous studies carried out in the macaque monkey found that lesions of the amygdala not only decrease emotional reactivity but also disrupt normal social interactions. We have re-investigated the relationship between amygdala lesions and social behavior in cohorts of mature and neonatal rhesus monkeys who were prepared with selective and complete bilateral ibotenic acid lesions of the amygdaloid complex. These animals display clear alterations in emotional and social behavior. We interpret these changes as due to a loss of the ability to evaluate environmental stimuli as potential threats. However, adult animals with bilateral lesions of the amygdala demonstrate near normal, and even increased, social interactions with conspecifics. Moreover, neonatal animals, prepared with amygdala lesions at 2 weeks of age, also demonstrate species typical social behaviors such as the generation of facial expressions, grooming and play behavior. These results argue against the idea that the amygdala is essential for the interpretation of social communication or for the expression of social behavior. Because it does appear to participate in the evaluation of the "safety" of social interactions, we believe that it does have a role in modulating the amount of social behavior in which an organism will participate. However, our current answer to the question posed in the title of this paper is no!

Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder

“…The inconsistent literature concerning amygdala structure in adults with BD, compared with consistent findings of decreased amygdala volume in pediatric BD, suggest that amygdala dysfunction in BD may vary developmentally. Such developmental variation would be consistent with data in nonhuman primates suggesting that amygdala lesions produce markedly different effects on emotional processes in immature relative to mature organisms (41).…”

Stereological analysis of the rat and monkey amygdala

“…However, the relatively small variations that might be induced by rearing conditions are very unlikely to account for the major differences in the morphological features, such as main amygdala nuclei volumes and neuron and glial cell numbers, observed between species. Moreover, the rearing conditions described here correspond to those typically employed in functional studies of the amygdala in rats (Pitkänen et al, 1997; LeDoux, 2000; Balleine and Killcross, 2006; Sigurdsson et al, 2007) and monkeys (Emery et al, 2001; Prather et al, 2001; Amaral et al, 2003; Bauman et al, 2004). …”

“…Thus, to illustrate the functional impact of these morphometric differences between species, let us consider that the amygdala serves essentially as a danger detector, in both rodents and primates, thus facilitating the survival of the individual animal. Although this survival function is essentially conserved in primates, because the primate amygdala can integrate additional contextual information, this additional information can further lead to the regulation of more complex behaviors such as the modulation of social interactions (Amaral et al, 2003). Going one step farther, as in the case of the human, where integration may be even greater, the amygdala is also activated when subjects are presented with untrustworthy faces (Adolphs et al, 1998; Winston et al, 2002), positive words (Hamann and Mao, 2002), happy faces (Canli et al, 2002), amusement-inducing movies (Aalto et al, 2002), and other complex social stimuli that might not have an equivalent in rodents.…”

“…Amygdala function has long been associated with emotional behavior, particularly fear (Davis, 2000; LeDoux, 2003; Feinstein et al, 2011), stress (Roozendaal et al, 2009), anxiety (Rauch et al, 2003), and appetitive and aversive conditioning (Shabel and Janak, 2009). The amygdala has also been linked to the neural systems that underlie normal social behavior (Adolphs, 2003), essentially via the modulation of fear (Emery et al, 2001; Prather et al, 2001; Amaral et al, 2003; Bauman et al, 2004). In addition, the amygdala has been shown to be important for the modulation of memory processes, particularly under arousing or emotionally salient conditions (McGaugh, 2004; Roozendaal et al, 2009).…”

“…In contrast, primates have been the model of choice for studies of the role of the amygdala in social behavior (Amaral et al, 2003; Adolphs, 2010). Several neuroanatomical studies, however, have already pointed out striking differences in the organization of the amygdaloid complex in rats, monkeys, and humans at the cellular level.…”