Social buffering ameliorates conditioned fear responses in female rats

Ishii, Akiko; Kiyokawa, Yasushi; Takeuchi, Yukari; Mori, Yuji

doi:10.1016/j.yhbeh.2016.03.003

Cited by 57 publications

(39 citation statements)

References 27 publications

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“…Previous studies have shown social buffering of anxiety and fear in rodents (Burkett et al, 2016; Hennessy et al, 2009; Kikusui et al, 2006; Waldherr and Neumann, 2007). Particularly relevant are the studies showing that male and female adult rats freeze less to a conditioned cue when in the presence of other male rats (Ishii et al, 2016; Kiyokawa et al, 2004, Kiyokawa et al, 2007). Hence, the decrease in freezing by mother rats reported here is unlikely to be specific to the presence of offspring.…”

Section: Discussionmentioning

confidence: 99%

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

Rickenbacher

Perry

Sullivan

et al. 2017

eLife

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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

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Section: Discussionmentioning

confidence: 99%

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

Rickenbacher

Perry

Sullivan

et al. 2017

eLife

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“…Studies in rodents, however, are predominantly performed on males, with only a few cases where female empathic abilities were investigated (Atsak et al, 2011; Ben-Ami Bartal et al., 2011; Ishii et al 2015; Jones et al, 2014; Langford et al, 2011; Mikosz et al 2015; Panksepp and Lahvis, 2016). Despite strong evidence suggesting the influence of menstrual cycle on empathy in women (Derntl et al, 2013, 2008; Guapo et al, 2009; Pearson and Lewis, 2005) only three of the aforementioned studies (Ishii et al 2015; Jones et al, 2014; Mikosz et al 2015) accounted for the estrous cycle of the studied females, and only the latter compared the obtained results also between the sexes. In that study, in the model of socially transferred fear, differences in active avoidance learning following the interaction with a stressed demonstrator were found between male (and diestral female) versus estral female observers.…”

Section: Sex Differencesmentioning

confidence: 99%

The roots of empathy: Through the lens of rodent models

Meyza

Bartal

Monfils

et al. 2017

Neuroscience & Biobehavioral Reviews

156

125

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Empathy is a phenomenon often considered dependent on higher-order emotional control and an ability to relate to the emotional state of others. It is, by many, attributed only to species having well-developed cortical circuits capable of performing such complex tasks. However, over the years, a wealth of data has been accumulated showing that rodents are capable not only of sharing emotional states of their conspecifics, but also of prosocial behavior driven by such shared experiences. The study of rodent empathic behaviors is only now becoming an independent research field. Relevant animal models allow precise manipulation of neural networks, thereby offering insight into the foundations of empathy in the mammalian brains. Here we review the data on empathic behaviors in rat and mouse models, their neurobiological and neurophysiological correlates, and the factors influencing these behaviors. We discuss how simple rodent models of empathy enhance our understanding of how brain controls empathic behaviors.

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“…First, we find sex does not modulate harm aversion. This is in apparent contrast to a small number of studies that reported sex effects on vicarious responses in mice [23,34] and rats [35,36], pointing towards a growing awareness that the specific output behavior measured can dramatically alter sex differences [37]. Second, the pain of the victim needs to be contingent on the actor's actions: the same number of shocks to the victim without contingency (RandomHarm condition does not change lever-preference.…”

Section: Discussionmentioning

confidence: 81%

Harm to others acts as a cingulate dependent negative reinforcer in rat

Hernandez-Lallement

Attah

Gazzola

et al. 2019

Preprint

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Empathy, the ability to share another individual's emotional state and/or experience, has been suggested to be a source of prosocial motivation by making actions that harm others aversive. The neural underpinnings and evolution of such harm aversion remain poorly understood. Here, we characterize an animal model of harm aversion in which a rat can choose between two levers providing equal amounts of food, but one additionally delivering a footshock to a neighboring rat. We find that independently of sex and familiarity, rats reduce their usage of the preferred lever when it causes harm to a conspecific, displaying an individually varying degree of harm aversion. Prior experience with pain increases this effect. In additional experiments, we show that rats reduce the usage of the harm-inducing lever when it delivers twice, but not thrice the number of pellets than the non-preferred lever, setting boundaries on the magnitude of harm aversion. Finally, we show that pharmacological deactivation of the anterior cingulate cortex, a region we have shown to be essential for emotional contagion, reduces harm aversion, while leaving behavioral flexibility unaffected. This model of harm aversion might help shed light onto the neural basis of psychiatric disorders characterized by reduced harm aversion, including psychopathy and conduct disorders with reduced empathy, and provide an assay for the development of pharmacological treatments of such disorders. Figure 1 | Experimental Procedures. (A) Photo of the cabinet in which the experimental set-up was isolated. (B) Top view of the two-compartment set-up. (C) View of the actor's compartment through the perforated transparent divider as seen from the victim's compartment. (D) Close-up of the left wall with one of the two levers and food hoppers available to the actor. (E) Timeline of the procedures. (F) Design of exposure, baseline, shock and reversal sessions. Note that the reversal session is only present in some conditions (Table 1, 2). During exposure, the actor receives 4 shocks alone in the victim compartment. During Baseline, pressing one lever (left column) or the other (right column) leads to one pellet for the actor. The lever preferred during baseline then additionally triggers a shock to the victim during the 3 days of the Shock phase. During reversal, shocks are no longer delivered, but the non-preferred lever now leads to 3 pellets. (G) Trial structure for training, baseline, shock and reversal sessions. Grey coloring denotes events and purple, the rat's responses. (H) Simulated distribution for switching (left) and reversal indexes (right) given their respective equations and uniform distributions of preferences. Dots and lines above the distributions are the median and the 25 and 75 % percentile. Figure 2 | Harm aversion in rats. (A) Percent choice for shock lever across sessions (Baseline, Shock1, Shock2and Shock3) and conditions (ContingentHarm, NoHarm and RandomHarm). The numbers above the graph specifie the t-statistic (t), one-tailed FDR corrected p (p1,F...

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Social buffering ameliorates conditioned fear responses in female rats

Cited by 57 publications

References 27 publications

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

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

The roots of empathy: Through the lens of rodent models

Harm to others acts as a cingulate dependent negative reinforcer in rat

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