Bidirectional cingulate-dependent danger information transfer across rats

Abstract

Social transmission of freezing behavior has been conceived of as a one-way phenomenon in which an observer “catches” the fear of another. Here, we use a paradigm in which an observer rat witnesses another rat receiving electroshocks. Bayesian model comparison and Granger causality show that rats exchange information about danger in both directions: how the observer reacts to the demonstrator’s distress also influences how the demonstrator responds to the danger. This was true to a similar extent across highly familiar and entirely unfamiliar rats but is stronger in animals preexposed to shocks. Injecting muscimol in the anterior cingulate of observers reduced freezing in the observers and in the demonstrators receiving the shocks. Using simulations, we support the notion that the coupling of freezing across rats could be selected for to more efficiently detect dangers in a group, in a way similar to cross-species eavesdropping.

Similar levels of emotional contagion in male and female rats

“…Based on the literature showing less freezing in females in non-social experiments 33,34 , and our own experiments showing lower levels of freezing in female observers and demonstrators in our emotional contagion tests compared to males (see 16 for females and 17,28,29 for females), we wanted to directly test the effect of sex on our emotional contagion test, and expected to find reduced freezing in females compared to males. This expectation was confirmed by our data.…”

“…However, the specific question of interest is whether there were sex differences in emotional contagion, the degree of affective alignment between two rats. Following up on our recent introduction of dyadic methods, that quantify the relationship between freezing behavior in observers and demonstrators 29 , here we leverage these methods to quantify emotional contagion as the strength of the link between the freezing behavior across the two members of each pair. We exploit two methods to do so.…”

“…Given that in the past we had run an experiment with only females 16 , and later several experiments with only males 17,28,29 , and observed higher levels of freezing in both male observers and male demonstrators than in our original female sample, we expected that females would show reduced levels of freezing compared to males in this experiment. However, when conceiving of emotional contagion as the link between the freezing of the two animals, would we find a stronger link in females than males?…”

“…Emotional contagion can be quantified systematically in rodents using designs in which one demonstrator animal receives a footshock, and the freezing of another observer that witnesses the event is found to be increased, suggesting that the distress of the shocked demonstrator was transferred to the observer 16,17,21,[24][25][26][27][28][29] . We have recently introduced ways to quantify emotional transfer in this paradigm by leveraging Bayesian statistics and Granger causality 29 . Here we therefore ask whether by using these quantification methods, emotional contagion is stronger in females compared to male Long Evans rats.…”

Transient uterine hypercontractility causes fetal cerebral oxidative stress and enduring mitochondrial and behavioral abnormalities in adolescent male rat offspring

“…We pursued this with evaluation of the expression of nrxn1, previously associated with social behavior, in brain regions known to be integral to the neurocircuitry of social interaction (amygdala, anterior cingulate cortex, somatosensory cortex). [42][43][44][45][46][47][48][49] Expression of nrxn1 was differentially regulated in the brain regions of OXT-exposed offspring regardless of the sex; nrxn1 was significantly downregulated in the amygdala, but unchanged in the anterior cingulate and the somatosensory cortices of OXT vs. control offspring. Because these results do not explain male-specific impairment of social behavior, we speculate that these changes could be due to sex differences in the response to oxidative stress.…”