Abstract
Recent studies in monkeys have demonstrated that damage to the lateral subfields of orbital frontal cortex (OFC areas 11/13) yields profound changes in flexible modulation of goal-directed behaviors and deficits in fear regulation. Yet, little consideration has been placed on its role in emotional and social development throughout life. The current study investigated the effects of neonatal lesions of the OFC on the flexible modulation of goal-directed behaviors and fear responses in monkeys. Infant monkeys received neonatal lesions of OFC areas 11/13 or sham-lesions during the first post-natal week. Modulation of goal-directed behaviors was measured with a devaluation task at 3–4 and 6–7 years. Modulation of fear reactivity by safety signals was assessed with the AX+/BX− fear-potentiated-startle paradigm at 6–7 years. Similar to adult-onset OFC lesions, selective neonatal lesions of OFC areas 11/13 yielded a failure to modulate behavioral responses guided by changes in reward value, but spared the ability to modulate fear responses in the presence of safety signals. These results suggest that these areas play a critical role in the development of behavioral adaptation during goal-directed behaviors, but not or less so, in the development of the ability to process emotionally salient stimuli and to modulate emotional reactivity using environmental contexts, which could be supported by other OFC subfields, such as the most ventromedial subfields (i.e., areas 14/25). Given similar impaired decision-making abilities and spared modulation of fear after both neonatal lesions of either OFC areas 11 and 13 or amygdala (Kazama et al., 2012; Kazama and Bachevalier, 2013), the present results suggest that interactions between these two neural structures play a critical role in the development of behavioral adaptation; an ability essential for the self-regulation of emotion and behavior that assures the maintenance of successful social relationships.
Highlights
The ability to process and flexibly respond to quickly changing social information requires the complex interaction between many brain areas, including the components of the orbitofrontolimbic circuit
The Group effect and the Group × Startle amplitude interactions did not reach significance [F = 2.37 and F = 1.42, all ps > 0.05, respectively], startle amplitudes across almost all noise intensities were slightly lower in animals with Neo-Oasp lesions than in sham-operated controls
SUMMARY OF EXPERIMENT 2 The data demonstrated that neonatal lesions of OFC areas 11 and 13 did not alter acquisition of the fear and safety cues, condition inhibition, and extinction
Summary
The ability to process and flexibly respond to quickly changing social information requires the complex interaction between many brain areas, including the components of the orbitofrontolimbic circuit. Cross-talk between the amygdala and the orbital frontal cortex is known to be critical for using cost-benefit information to guide optimal decisionmaking (see Murray and Wise, 2010, for review). This conclusion is based on several tract-tracing studies demonstrating strong bidirectional connections between the amygdala and the orbital frontal cortex in the non-human primate brain (see Barbas, 2000; Ongur and Price, 2000 for review). There is a growing need to better define the critical role of the orbital frontal cortex and amygdala in the ability to make appropriate decisions and to flexibly regulate behavior during development
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