Neural circuit plasticity transforms infant neglect into maternal care
Chloe J Bair-Marshall1,2,3,4, Naomi L Cassel1,2,3,4,5, Ayat A Agha1,2,3,4
1Neuroscience Institute, New York University School of Medicine, New York, NY 10016 USA.
Infants in distress evoke strong emotional responses in adults, which help to elicit caretaking behaviors from parents to ensure infant needs are met1-3. However, neonatal care can also be challenging, and interactions with infants can lead to stress and negative affect even in potential caregivers4-7. Child neglect and maltreatment rates in human populations make it important to understand the neural mechanisms of regulating negative emotions and stress in the parental brain8-10. Here we show how rapid plasticity in female mouse central amygdala (CeA) transforms infant aversion into attentiveness after initial pup experience. Projections from CeA to locus coeruleus (CeA→LC) were strongly activated upon initial pup contact leading to pup aversion. CeA→LC pup responses were reduced with parental experience and down-regulating CeA→LC activity led to less aversion. Oxytocin signaling in central amygdala was required to switch pup aversion to attention, inducing rapid long-term depression of excitatory inputs onto projection neurons. CeA→LC projectors released the stress hormone corticotropin-releasing factor onto LC neurons, modulating phasic firing to regulate attention. This circuit organization enables local CeA computations of pup valence to be broadcast throughout the brain by the LC central arousal system, leading to appropriate pup-directed behaviors depending on adult state.
Infants in distress evoke strong emotional responses in adults, which help to elicit caretaking behaviors from parents to ensure infant needs are met1-3. However, neonatal care can also be challenging, and interactions with infants can lead to stress and negative affect even in potential caregivers4-7. Child neglect and maltreatment rates in human populations make it important to understand the neural mechanisms of regulating negative emotions and stress in the parental brain8-10. Here we show how rapid plasticity in female mouse central amygdala (CeA) transforms infant aversion into attentiveness after initial pup experience. Projections from CeA to locus coeruleus (CeA→LC) were strongly activated upon initial pup contact leading to pup aversion. CeA→LC pup responses were reduced with parental experience and down-regulating CeA→LC activity led to less aversion. Oxytocin signaling in central amygdala was required to switch pup aversion to attention, inducing rapid long-term depression of excitatory inputs onto projection neurons. CeA→LC projectors released the stress hormone corticotropin-releasing factor onto LC neurons, modulating phasic firing to regulate attention. This circuit organization enables local CeA computations of pup valence to be broadcast throughout the brain by the LC central arousal system, leading to appropriate pup-directed behaviors depending on adult state.
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