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Genes Brain Behav. 2016 Jan;15(1):144-54. doi: 10.1111/gbb.12261. Epub 2015 Nov 13.

Developmental emergence of fear/threat learning: neurobiology, associations and timing.

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Institut des Neurosciences Paris Saclay (Neuro-PSI), UMR 9197, CNRS/Université Paris-Sud, Orsay, France.
Emotional Brain Institute, The Nathan S. Kline Institute for Psychiatric Research, Orangeburg.
Child Study Center Institute for Child and Adolescent Psychiatry, New York University Langone Medical Center, New York, NY, USA.


Pavlovian fear or threat conditioning, where a neutral stimulus takes on aversive properties through pairing with an aversive stimulus, has been an important tool for exploring the neurobiology of learning. In the past decades, this neurobehavioral approach has been expanded to include the developing infant. Indeed, protracted postnatal brain development permits the exploration of how incorporating the amygdala, prefrontal cortex and hippocampus into this learning system impacts the acquisition and expression of aversive conditioning. Here, we review the developmental trajectory of these key brain areas involved in aversive conditioning and relate it to pups' transition to independence through weaning. Overall, the data suggests that adult-like features of threat learning emerge as the relevant brain areas become incorporated into this learning. Specifically, the developmental emergence of the amygdala permits cue learning and the emergence of the hippocampus permits context learning. We also describe unique features of learning in early life that block threat learning and enhance interaction with the mother or exploration of the environment. Finally, we describe the development of a sense of time within this learning and its involvement in creating associations. Together these data suggest that the development of threat learning is a useful tool for dissecting adult-like functioning of brain circuits, as well as providing unique insights into ecologically relevant developmental changes.


Amygdala; Pavlovian conditioning; aversive conditioning; contextual learning; corticosterone; interval timing; neural circuits; ontogeny; pup

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