Natural variations in maternal care in the rat influence the development of neuronal systems that regulate endocrine and behavioral responses to stress. Thus, as adults, rats that received higher levels of maternal licking/grooming (LG) in infancy are less 'fearful' in response to novelty, compared with adult offspring of Low LG mothers. The present study examined the influence of maternal care on behavioral and neuronal responses to a more specific, localizable form of threat using an electrified probe in the shock-probe burying test. Even under these conditions, adult offspring of High LG mothers displayed lower levels of fear reactivity (i.e. less shock-induced freezing and probe burying) throughout the test than did offspring of Low LG mothers. These differences in fearfulness were associated with differential patterns of cFos immunoreactivity (cFos-IR), 120 min following test exposure. Relative to control rats exposed to a non-electrified probe, cFos-IR was increased in the offspring of High LG mothers exposed to an electrified probe in the dentate gyrus, ventral subiculum, lateral and medial septum, nucleus accumbens and the dorsal periaqueductal gray. Shock-exposed offspring of Low LG dams displayed a very different pattern of neuronal activation characterized by both increases (area CA1 of the ventral hippocampus and the inferior colliculus) and decreases (paraventricular nucleus of the hypothalamus and the ventrolateral periaqueductal gray) in cFos-IR compared with the no-shock controls. Together these results suggest that maternal care serves to 'program' neuronal circuits that modulate fear-related responding in the rat resulting in qualitatively different neuronal responses to stress.