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

Abstract

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.

The Impact of Early Amygdala Damage on Juvenile Rhesus Macaque Social Behavior

“…During interactions both with familiar and novel animals, in dyads and social groups, amygdala-lesioned animals expressed more signs of fear or submission (e.g., grimacing, screaming, etc.). This latter observation stands in contrast to the typical pattern of social behaviors generated by animals that receive amygdala damage as adults (i.e., less signaling of fear; Emery et al 2001; Machado et al, 2008). The goal of this study was to continue the evaluation of juvenile macaque social behavior following neonatal damage to the amygdala or hippocampus, at a later developmental point during which the animals were living in a more socially enriched environment.…”

“…Lesion placement was confirmed via (1) T2-weighted MR images acquired 10 days after surgery, (2) T1-weighted images acquired when the animals were approximately 4 years (Machado, Snyder, Cherry, et al, 2008), and (3) histological analysis of the one amygdala-lesioned subject who died during his first year of life. First, edema associated with the brain lesions was measured using T2-weighted MR images collected 10 days post-surgery using a General Electric 1.5 T Gyroscan magnet (slice thickness=1.5 mm thick; T2 weighted Inversion Recovery Pulse sequence: repetition time = 4000, echo time = 102, NEX 3, field of view = 8 cm, matrix, 256 × 256).…”

“…T2-weighted images of coronal sections through the mid portion of the amygdala are illustrated in previous publications (Bauman et al, 2004a, 2004b; Bliss-Moreau, Bauman, & Amaral, 2011), indicating that the ibotenic acid was injected into and caused damage to the amygdala or hippocampus. Second, lesion extent was further characterized in T1-weighted MRI images when animals were 4 years (Machado, Snyder, Cherry, et al, 2008). Finally, the extent of the targeted lesion was confirmed using histological evaluation in the one amygdala-lesioned animal that died due to an unrelated illness.…”

“…Damage to the adult primate amygdala disrupts affective processing (e.g., Aggleton & Passingham, 1981; Zola-Morgan et al, 1991; Meunier, et al, 1999; Stefanaci, Clark & Zola, 2003; Izquierdo, Suda & Murray, 2005; Mason et al, 2006; Machado et al, 2009; Chudasama, Izquierdo & Murray, 2009 Antoniadis, Winslow, Davis & Amaral, 2007; 2009) which has consequences for social behavior when interacting with conspecifics (e.g., Rosvold, Mirsky, & Pribram, 1954; Mirsky, 1960; Kling, 1974; Emery et al, 2001; Machado & Bachevalier, 2006; Machado et al, 2008). Changes in social behavior observed in animals with adult amygdala damage have been hypothesized to result from disruption of danger detection functions of the amygdala (Amaral, 2006) rather than to an alteration to social behavior per se.…”

“…Changes in social behavior observed in animals with adult amygdala damage have been hypothesized to result from disruption of danger detection functions of the amygdala (Amaral, 2006) rather than to an alteration to social behavior per se. In this view, adult amygdala-lesioned animals are hypersocial (Emery et al, 2001; Machado et al, 2008) because they fail to process the potential threat of novel conspecifics. In other words, they do not demonstrate the species-typical reluctance to engage a novel conspecific in social interaction before clear dominance relationships are established.…”