Freezing suppression by oxytocin in central amygdala allows alternate defensive behaviours and mother-pup interactions

Abstract

When animals and their offspring are threatened, parents switch from self-defense to offspring protection. How self-defense is suppressed remains elusive. We postulated that suppression of the self-defense response, freezing, is gated via oxytocin acting in the centro-lateral amygdala (CeL). We found that rat dams conditioned to fear an odor, froze when tested alone, whereas if pups were present, they remained in close contact with them or targeted the threat. Furthermore, blocking oxytocin signaling in the CeL prevented the suppression of maternal freezing. Finally, pups exposed to the odor in the presence of the conditioned dam later froze when re-exposed alone. However, if oxytocin signaling in the dam had been blocked, pups failed to learn. This study provides a functional role for the well-described action of oxytocin in the central amygdala, and demonstrates that self-defense suppression allows for active pup protection and mother-pup interactions crucial for pup threat learning.DOI: http://dx.doi.org/10.7554/eLife.24080.001

Role of oxytocin in the control of stress and food intake

“…24 Recently, oxytocin has been shown to reduce passive coping behaviour such as freezing behaviour by acting on neurones in the lateral part of the central amygdala, which inhibits the activity of periaqueductal gray-projecting central amygdala neurones, and, as a result, induces active escape behaviour 106 or active defensive behaviour. 269 Consistent with this idea, oxytocin has been shown to suppress social loss-induced passive coping behaviour in male prairie voles 84 and to induce social defeat-induced risk assessment behaviour (head orientation) in female mice by acting on the bed nucleus of the stria terminalis. 12,270 Furthermore, oxytocin facilitates expression of social defeat posture, which is an active coping behaviour showing subordination toward dominant conspecifics, by possibly acting on the ventromedial hypothalamus or periaqueductal gray in male mice.…”

Acute and long-lasting effects of oxytocin in cortico-limbic circuits: consequences for fear recall and extinction

“…For instance, we have found that, although OT does decrease freezing when released in the CeA, it is without effect on other parameters of fear, especially heart rate variability (Viviani et al 2011). Instead, OT might induce a switch from passive to active defensive behavior as demonstrated in lactating mothers (Bosch et al 2005;Rickenbacher et al 2017), in the presence of social stimuli. Thus, there is still a lot to be discovered about the role of OT in anxiety-like behavior, not in the least about plastic long-lasting changes in the corticolimbic fear memory circuits.…”

“…Therefore, we propose that putative contributions of OT to neuronal plasticity in the fear retrieval and extinction circuits can be best studied in relation to social interactions. In agreement with this, OT is released in the CeA in lactating mother rats in the presence of their pups (i.e., a social stimulus) to reduce freezing and increase active defensive behavior to protect the pups (Rickenbacher et al 2017). The proof of whether OT release under socially relevant conditions induces plastic changes in the circuits of fear extinction is thus an attractive question waiting to be answered.…”

Behavior: Oxytocin Promotes Fearless Motherhood

“…By activating local inhibitory interneurons, the enhanced release of oxytocin inhibits neural activity in the LS, subsequently attenuating fear responses of mothers. The study of Menon et al echoes a recently published study in rats [14], where the authors used odor fear conditioning to show that oxytocin acts in the central amygdala to prevent fearinduced freezing response in lactating mothers, thus enabling them to actively protect their pups. Together, both of these studies show how oxytocin modulates brain activity to prevent an adaptive fear response, such as freezing, in situations where it could possibly be maladaptive, such as when mothers protect their offspring.…”