Effects of Neonatal Amygdala Lesions on Fear Learning, Conditioned Inhibition, and Extinction in Adult Macaques

• Type of Material: Article
• Authors: Andrew M. Kazama, Emory University; Eric Heuer, Emory University; Michael E Davis, Emory University; Jocelyne Bachevalier, Emory University
• Language: English
• Date: 2012-06
• Publisher: American Psychological Association
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2012 American Psychological Association 2012
• Final Published Version (URL): http://www.apa.org/
• Title of Journal or Parent Work: Behavioral Neuroscience
• ISSN: 0735-7044
• Volume: 126
• Issue: 3
• Start Page: 392
• End Page: 403
• Grant/Funding Information: This work was supported by grants from the National Institute of Mental Health (MH-58846, MH-086947, and MH-047840), the National Institute of Child Health and Human Development (HD-45471), Yerkes base grant (RR-00165), and the Autism Speaks Pre-doctoral Fellowship Grant.
• Keywords: emotion regulation; safety-signal learning; post-traumatic stress disorder; rhesus monkey
• Research Categories: Biology, Neuroscience; Psychology, Behavioral

Abstract

Fear conditioning studies have demonstrated the critical role played by the amygdala in emotion processing. Although all lesion studies until now investigated the effect of adult-onset damage on fear conditioning, the current study assessed fear-learning abilities, as measured by fear-potentiated startle, in adult monkeys that had received neonatal neurotoxic amygdala damage or sham-operations. After fear acquisition, their abilities to learn and use a safety cue to modulate their fear to the conditioned cue, and, finally, to extinguish their response to the fear conditioned cue were measured with the AX+/BX− Paradigm. Neonatal amygdala damage retarded, but did not completely abolish, the acquisition of a learned fear. After acquisition of the fear signal, four of the six animals with neonatal amygdala lesions discriminated between the fear and safety cues and were also able to use the safety signal to reduce the potentiated-startle response and to extinguish the fear response when the air-blast was absent. In conclusion, the present results support the critical contribution of the amygdala during the early phases of fear conditioning that leads to quick, robust responses to potentially threatening stimuli, a highly adaptive process across all species and likely to be present in early infancy. The neonatal amygdala lesions also indicated the presence of amygdala-independent alternate pathways that are capable to support fear learning in the absence of a functional amygdala. This parallel processing of fear responses within these alternate pathways was also sufficient to support the ability to flexibly modulate the magnitude of the fear responses.