Testosterone can foster friendly, prosocial behavior in males, a new animal study finds. The Proceedings of the Royal Society B published the research on Mongolian gerbils conducted by neuroscientists at Emory University.
“For what we believe is the first time, we’ve demonstrated that testosterone can directly promote nonsexual, prosocial behavior, in addition to aggression, in the same individual,” says Aubrey Kelly, Emory assistant professor of psychology and first author of the study.
“It’s surprising because normally we think of testosterone as increasing sexual behaviors and aggression. But we’ve shown that it can have more nuanced effects, depending on the social context.”
Richmond Thompson, a neuroscientist at Oxford College of Emory University, is co-author of the study.
Kelly’s lab has recently focused on the neural effects of oxytocin using rodent experimental models. Thompson’s lab investigates the neural effects of steroids in fish. Both scientists are trying to get at the question of how hormones work in the brain to allow an animal to rapidly change its behavior, depending on the social context.
In addition to sharing this research interest, Kelly and Thompson share a home as a married couple.
“The idea for this paper was borne out of us talking together over a glass of wine,” Kelly says. “It blends our two research worlds.”
The majority of human studies show that testosterone enhances aggressive behavior. Kelly and Thompson wondered if maybe testosterone might, in lockstep with being able to increase aggression toward intruders, also generally dampen prosocial behaviors.
However, they also hypothesized that it might do something more radical — actually enhance positive social responses in contexts in which acting prosocially is appropriate.
To test this question, the Kelly lab conducted experiments on Mongolian gerbils, rodents that form lasting pair bonds and raise their pups together. While males can become aggressive during mating and in defense of their territory, they also exhibit cuddling behavior after a female becomes pregnant, and they demonstrate protective behavior toward their pups.
In one experiment, a male gerbil was introduced to a female gerbil. After they formed a pair bond and the female became pregnant, the males displayed the usual cuddling behaviors toward their partners.
The researchers then gave the male subjects an injection of testosterone. They expected that the resulting acute rise in a male’s testosterone level would lessen his cuddling behaviors if testosterone generally acts as an antisocial molecule.
“Instead, we were surprised that a male gerbil became even more cuddly and prosocial with his partner,” Kelly says. “He became like ‘super partner.’”
In a follow-up experiment a week later, the researchers conducted a resident-intruder test. The females were removed from the cages so that each male gerbil that had previously received a testosterone injection was alone in his home cage. An unknown male was then introduced into the cage.
“Normally, a male would chase another male that came into its cage, or try to avoid it,” Kelly says. “Instead, the resident males that had previously been injected with testosterone were more friendly to the intruder.”
The friendly behavior abruptly changed, however, when the original male subjects were given another injection of testosterone. They then began exhibiting normal chasing and/or avoidance behaviors with the intruder.
“It was like they suddenly woke up and realized they weren’t supposed to be friendly in that context,” Kelly says.
The researchers theorize that because the male subjects experienced a surge in testosterone while they were with their partners, it not only rapidly increased positive social responses toward them but also primed the males to act more prosocially in the future, even when the context changed and they were in the presence of another male.
However, the second testosterone injection then rapidly prompted them to switch their behavior to become more aggressive, as appropriate to the context of a male intruder.
The laboratory experiments, in a sense, slowed down what the males might experience almost simultaneously in the wild. In their natural habitat, Kelly explains, mating with a partner elevates testosterone, which primes them to act cuddly in the moment and in the near future while living with their partner, even if the testosterone levels decline.
If a rival entered its burrow the gerbil would likely experience another surge of testosterone that would immediately help adjust his behavior so he can fend off the rival and protect his pups. Testosterone, then appears to help animals rapidly pivot between prosocial and antisocial responses as the social world changes.
The current study also looked at how testosterone and oxytocin interact biologically. The results showed that the male subjects receiving injections of testosterone exhibited more oxytocin activity in their brains during interactions with a partner compared to males that did not receive the injections.
“We know that systems of oxytocin and testosterone overlap in the brain but we don’t really understand why,” Kelly says. “Taken together, our results suggest that one of the reasons for this overlap may be so they can work together to promote prosocial behavior.”
Rather than just flipping an “on” or “off” button to modulate behaviors, hormones seem to play a more nuanced role, Kelly says. “It‘s like a complicated dashboard where one dial may need to move up a bit while another one moves down.”
Human behaviors are far more complex than those of Mongolian gerbils, but the researchers hope that their findings provide a basis for complementary studies in other species, including humans.
“Our hormones are the same, and the parts of the brain they act upon are even the same,” Thompson says.
“So, learning how hormones like testosterone help other animals adjust to rapidly changing social contexts will not only help us understand the biological nuts and bolts that affect their behavior, but also predict and ultimately understand how the same molecules in human brains help shape our own responses to the social world around us.”
Jose Gonzalez Abreu, a former research specialist in the Kelly lab, is a co-author of the study.
In this study, we sought to expand on what is known about the influence of testosterone on male social behavior. Although empirical research and popular opinion center on its role in driving aggressive and antisocial behaviors, direct causal evidence for this link is weak in men (11, 12, 35). Some have suggested (12, 28, 29) that testosterone instead promotes both aggressive and nonaggressive behaviors that enhance and maintain social status.
Here, we experimentally manipulated the testosterone levels of young males and tested the fundamental predictions of these theories against behavior in a two-player economic bargaining game.
We found that administration of testosterone caused participants to punish their opponents more frequently than those administered placebo and that higher testosterone levels were specifically associated with increased punishment of opponents who made unfair offers.
Importantly, this punishment was costly to the participant and could not be used as an instrument to coerce their opponent into offering them larger amounts, because their opponents’ behavior was known by participants to be predetermined. Thus, unlike previous studies, we can conclude that testosterone can indeed cause male aggression (13) and that this aggression was not mediated by an increased motivation to maximize task earnings or altered beliefs about the strategic influence of their actions on others (33).
Testosterone has been suggested to selectively potentiate aggression that is reactive, or in response to provocation (30). Our results support such an interpretation, showing that, in the absence of provocation, as when they received large offers, participants in the treatment group were not less likely to reward these offers than those in the control group. Rather than giving rise to indiscriminate aggression, testosterone seemed to intensify aggression in social contexts where social status may be under threat. This effect is consistent with the idea that testosterone-induced aggression may be a tool to achieve social dominance and garner reproductive opportunities (13).
However, our results indicate that testosterone’s influence on male social behavior is not limited to reactive aggression. Participants who received testosterone were in fact more likely to offer monetary rewards to proposers who offered them large amounts of money. Furthermore, they chose rewards of greater magnitude than those administered placebo.
Again, the task design excludes the possibility that this behavior can be interpreted as being motivated by a strategic intention to influence their opponents’ future offers. This increase in generosity represents a demonstration that testosterone can cause male behavior that is prosocial or beneficial to others. In addition, this behavior satisfies a distinguishing prediction of the status theory of testosterone (28), namely that testosterone should stimulate nonaggressive behaviors in males if, like generosity, those behaviors are status enhancing.
The increase that we observe in both punishment of small offers and reward of large offers may raise the concern as to whether administration of testosterone caused participants to simply become more impulsive. However, we found that our treatment had no effect on the immediate decision of whether to reject the offer, which they made before deciding whether to punish or reward the proposer.
Treatment with testosterone also had no effect on the speed with which participants chose to punish or reward the proposer (SI Results, Fig. S5, and Table S5). The absence of an effect on reaction times suggests that testosterone does not simply enhance general emotional responsiveness but has a more restricted effect that is consistent with increasing status-enhancing aggressive and nonaggressive behaviors.
The increase that we observe in reward of large offers does not seem to result from an enhancement of their hedonic value, because participants treated with testosterone do not accept large offers more frequently or more rapidly than those treated with placebo. The choices of participants’ between monetary gambles in the nonsocial certainty equivalents task were also unaffected by treatment. Thus, it seems that testosterone specifically altered the social motivations underlying participants’ behavior.
Although the double-blind, placebo-controlled treatment procedure is a vital tool for determining whether hormones exert a causal influence on human behavior (28), it is not without potential limitations. We performed a number of precautionary analyses not previously used in the literature to determine the robustness of our results.
First, testosterone is converted to the estrogen estradiol by aromatase, which has led to suggestions that some effects of testosterone administration may be mediated by raised estradiol levels and not by testosterone per se (34, 36). We found that, in addition to raising their levels of testosterone, administering testosterone to our participants indeed caused a concomitant rise in their estradiol levels.
However, by including participants’ hormone levels as covariates in our behavioral analyses, we confirmed that greater punishment of unfair offers and reward of generous ones are attributable to participants’ testosterone levels and not to their levels of estradiol. In fact, the effects of estradiol were antagonistic to those of testosterone, with increased estradiol levels associated with a reduction in the rate and magnitude of both punishment of unfair offers and reward of generous offers.
Second, we show that high levels of testosterone among those in the placebo group were associated with higher rates of both punishment of proposers who made low offers and greater generosity toward those who made large offers, showing that the behavioral effects that we observe are not limited to the supraphysiological levels of testosterone caused by our treatment.
It should be noted that, although correlating participants’ choices with their peripheral levels of testosterone and estradiol provides insight into the role of each in driving behavior, future research on testosterone would benefit from the use of a hormonal manipulation that does not perturb estradiol levels. One possibility for future studies would be to suppress the conversion of testosterone to estradiol with the administration of an aromatase inhibitor.
Although this study is one of the only placebo-controlled pharmacological studies focusing on the role of testosterone in male behavior, the effects of testosterone on women’s behavior have received considerably more experimental attention (12, 37–39). It has been argued that testosterone may also promote status concerns in women (33, 39, 40), and a number of studies has shown that testosterone’s effects in women are not limited to promoting aggression (38–40).
In fact, our study extends to men recent findings suggesting that testosterone has important prosocial effects by increasing cooperation in the public goods game (38) and increasing generosity when repaying trust (39). There is some evidence, however, that there may be sex differences in the effects of testosterone.
Although in males, testosterone has been associated with decreased UG offers (10), administering testosterone to women increases (39) or does not change (37) UG offers. In addition, sex differences have been observed in the responsiveness of testosterone levels to social stimuli (41).
These findings may reflect fundamental differences in the function of testosterone in men and women or differences between the genders in the behaviors that are considered to increase status (42). Alternatively, we suggest that, in the light of our results, some of the sex variability in the effects of testosterone may be attributable to typically unmeasured effects of estradiol.
Neuroimaging studies have associated elevated testosterone with exaggerated blood oxygen level dependent (BOLD) responses in amygdala (43–45) and decreased amygdala–orbitofrontal cortex (OFC) coupling during processing of angry and fearful facial expressions (46, 47), with these mechanisms being suggested to mediate recruitment of aggressive behavior by testosterone in response to such threatening social stimuli (48).
One interesting question for future research is whether this pathway may also mediate the prosocial effects of testosterone that we observed given that the roles of amygdala and OFC in regulating social behavior are not limited to aggression (49, 50). Estrogen receptors are also known to be present in amygdala and other components of the reward system (51, 52), suggesting that testosterone and estradiol might influence behavior by binding to their respective receptors in the same set of neural structures.
Alternatively, given the opposing behavioral effects of estradiol and testosterone in this task, estradiol may have influenced behavior in the task by reducing the activity of androgen receptors by binding to the receptor (53) or down-regulation of receptor expression (54, 55).
Evolutionary game theories have established how the combination of two types of incentives (rewards and punishments) is efficient to lead to a population where defectors are punished and cooperation is promoted (56). Our study suggests that testosterone, by playing on both positive and negative incentives, could have played a key evolutionary role in not only promoting aggressive behavior but also, increasing generous behavior to maintain a high social status. Observations in nonhuman primates also indicate that the social hierarchy may be maintained by alpha males—having higher testosterone levels (57)—by not only aggressive behavior but also, sharing resources, such as access to food and females.
Our findings flatly contradict a simple link between testosterone and male aggression, a theory that would have predicted increased rejection and punishment of unfair offers and reduced reward of generous offers in those who had received testosterone. Instead, we find that testosterone’s effect on male behavior depended on the social context, and we show in a single experiment that testosterone can enhance both reactive aggression and generosity. This pattern of behavior cannot be explained by altered strategic beliefs (33) and is consistent with testosterone’s proposed role in promoting male behaviors that will increase social status (58), providing causal evidence for this theory.
reference link :https://www.pnas.org/doi/full/10.1073/pnas.1608085113#sec-3
Original Research: Closed access.
“Beyond sex and aggression: testosterone rapidly matches behavioral responses to social context and tries to predict the future” by Aubrey Kelly et al. Proceedings of the Royal Society B