Biology subjects

Heinemans, M.

Publications and source records attributed to Heinemans, M..

5 recordsLinked to original sources

bioRxiv2026

Neuronal sex identity shapes social buffering of defensive freezing behaviour in fruit flies

Sex differences are pervasive across the animal kingdom1,2, shaped by reproductive strategies, ecological roles, and physiological demands. Neurobiological studies have largely focused on sex differences in reproduction and aggression3,4, leaving understudied how sex shapes other survival-relevant behaviours such as responses to predatory threats. Previous work in vertebrates uncovered sex differences in individual defence responses deployed by rats5 and in social modulation of freezing responses in zebrafish6. The origin of these differences and their potential underlying neuronal circuitry remain however unknown. Here we characterise defensive responses to a visual threat of female and male fruit flies tested alone and in groups. Individually, defensive responses are comparable across sex, with similar freezing levels and moderately increased escape responses in males. In groups, however, we uncovered strong sex differences in freezing as males show consistently shorter freezing bouts, reflecting a stronger social buffering effect than in females. Using a generalised linear mixed model, we demonstrate that the shorter freezes of male flies, when tested in groups, are not explained by well-known locomotor differences between sexes7,8. Although males move more and faster, generating stronger social motion cues that mediate the "safety in numbers" effect in female flies9,10, their response to the surrounding motion is not increased. We further identify the nervous system as the source of this sex-dimorphic behaviour by feminising males through pan-neuronal ectopic expression of transformer, a key regulator of the cell-autonomous sex-differentiation pathway. Finally, we ruled out the visual projection neurons, lobula columnar neurons 11 (LC11), detectors of social motion10, as the source of the neuronal-sex differences observed. This study identifies a neuronal origin of sex differences in socially modulated behaviour that extends beyond sex-specific behavioural modules or locomotor function, important to understand differential impact on survival upon threat across sexes.

neuroscience↗

bioRxiv2022

Social cues of safety can override differences in threat level

Animals in groups integrate social information with that directly-gathered about the environment to guide decisions regarding reproduction, foraging and defense against predatory threats. In the context of predation, usage of social information has acute fitness benefits, aiding the detection of predators, the mounting of concerted defensive responses, or allowing the inference of safety, permitting other beneficial behaviors such as foraging for food. Individual and group defense responses to predatory threats can vary in modality and vigor depending on the perceived threat level. Moreover, predation level has been shown to modulate the use of social cues about foraging sites. Whether and how different threat levels affect the use of social cues to guide defense responses, is currently unknown. We previously showed that Drosophila melanogaster display a graded decrease in freezing behavior, triggered by an inescapable visual threat, with increasing group sizes. Crucially, we identified the movement of others as a cue of safety and its cessation a cue of threat and found the group responses to be primarily guided by the safety cues, resulting in a net social buffering effect. Here, we investigated how threat level impacts the use of social cues by exposing flies individually and in groups to two threat imminences using looms of different speeds. We show that freezing responses are stronger to the faster looms regardless of social condition. However, social buffering was stronger for groups exposed to the fast looms, such that the increase in freezing caused by the higher threat was less prominent in flies tested in groups than those tested individually. Through artificial control of behavior, we created different group compositions, titrating the motion cues that were maintained across threat levels. We, found that the same level of safety motion cues had a bigger weight on the flies decisions when these were exposed to the higher threat, thus overriding differences in perceived threat levels. These findings shed light on the safety in numbers effect, revealing the modulation of the saliency of social safety cues across threat intensities, a possible mechanism to regulate costly defensive responses.

neuroscience↗

bioRxiv2022

Looming stimuli reliably drive innate, but not learned, defensive responses in rats.

Survival relies on an organisms intrinsic ability to instinctively react to stimuli such as food, water, and threats, ensuring the fundamental ability to feed, drink, and avoid danger even in the absence of prior experience. These natural, unconditioned stimuli can also facilitate associative learning, where pairing them consistently with neutral cues will elicit responses to those cue. Threat conditioning, a well-explored form of associative learning, commonly employs painful electric shocks, mimicking injury, as unconditioned stimuli. It remains elusive whether actual injury or pain is necessary for effective learning, or whether the threat of harm is sufficient. Approaching predators create looming shadows and sounds, triggering strong innate defensive responses like escape and freezing. This study investigates whether visual looming stimuli can induce learned freezing or learned escape responses to a conditioned stimulus in rats. Surprisingly, pairing a neutral tone with a looming stimulus only weakly evokes learned defensive responses, in contrast to the strong responses observed when the looming stimulus is replaced by a shock. This dissociation sheds light on the boundaries for learned defensive responses thereby impacting our comprehension of learning processes and defensive strategies.

animal behavior and cognition↗

bioRxiv2019

Freezing displayed by others is a learned cue of danger resulting from co-experiencing own-freezing and shock

Social cues of threat are widely reported [1-3], whether actively produced to trigger responses in others, such as the emission of alarm calls, or by-products of an encounter with a predator, like the defensive behaviors themselves, such as an escape flight [4-14]. Although the recognition of social alarm cues is often innate [15-17], in some instances it requires experience to trigger defensive responses [4,7]. One mechanism proposed for how learning from self-experience contributes to social behavior is that of auto-conditioning, whereby subjects learn to associate their own behaviors with the relevant trigger events. Through this process the same behaviors, now displayed by others, gain meaning. [18,19 but see: 20]. Although it has been shown that only animals with prior experience with shock display observational freezing [21-25] suggesting that auto-conditioning could mediate this process, evidence for this hypothesis was lacking. Previously we found that when a rat freezes, the silence that results from immobility triggers observational freezing in its cage-mate, provided the cage-mate had experienced shocks before [24]. Hence, in our study auto-conditioning would correspond to rats learning to associate shock with their own response to it - freezing. Using a combination of behavioral and optogenetic manipulations, here we show that freezing becomes an alarm cue by a direct association with shock. Our work shows that auto-conditioning can indeed modulate social interactions, expanding the repertoire of cues that mediate social information exchange, providing a framework to study how the neural circuits involved in the self-experience of defensive behaviors overlap with the ones involved in socially triggered defensive behaviors.

animal behavior and cognition↗

bioRxiv2018

Cingulate dependent social risk assessment in rats

Social transmission of distress has been conceived of as a one-way phenomenon in which an observer catches the emotions of another. Here we use a paradigm in which an observer rat witnesses another receive electro-shocks. Bayesian model comparison and Granger causality argue against this one-way vision in favor of bidirectional information transfer: how the observer reacts to the demonstrators distress influences the behavior of the demonstrator. Intriguingly, this was true to a similar extent across highly familiar and entirely unfamiliar rats. Injecting muscimol in the anterior cingulate of observers reduced freezing in the observers and in the demonstrators receiving the shocks. That rats share the distress of unfamiliar strains is at odds with evolutionary thinking that empathy should be biased towards close individuals. Using simulations, we support the complementary notion that distress transmission could be selected to more efficiently detect dangers in a group.

neuroscience↗