Generalization of Conditioned Auditory Fear is Regulated by Maternal Effects on Ventral Hippocampal Synaptic Plasticity

Maternal care shapes individual differences in fear-associated neural circuitry. In rats, maternal licking and grooming (LG) in early life regulates ventral hippocampal (VH) function and plasticity in adulthood, but its consequent effect on the regulation of fear memories remains unknown. We report an effect of maternal care on generalization of learned fear, such that offspring of high LG mothers express generalized fear responses when confronted with neutral stimuli following auditory fear conditioning. These animals simultaneously display a reduction in the magnitude of VH long-term potentiation (LTP) expressed and reduced input–output transformation in Schaffer collateral synapses. Inhibition of VH-LTP during learning specifically increases fear generalization in offspring of low LG mothers during recall, suggesting a role for VH synaptic plasticity in the specification of fear memories. These findings suggest that rearing by low LG dams enhances the efficacy of fear-related neural systems to support accurate encoding of fear memories through effects on the VH.