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Moita, M. A.

Publications and source records attributed to Moita, M. A..

8 recordsLinked to original sources

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↗

Covert muscle activity reveals dynamic freezing states and prepares the animal for action

When an animal detects a threat it must make a split-second choice between fight, flight or freezing (1-3). During freezing, skeletal muscles sustain tension to maintain rigid, sometimes atypical postures, for many minutes at a time (4). Meanwhile the animal must dynamically assess its surroundings to plan future actions and ready its body for movement. The interplay between the neural and somatic systems during freezing remains poorly understood. Here we show that freezing Drosophila melanogaster display a striking novel pattern of leg muscle activation unique to immobility, a rhythmic pulsing in the distal tibia. The muscle, which we show to be a previously undescribed leg accessory heart, displays multiple activity modes and ramps up to movement onset, implying a preparation for movement. The frequency of pulsing is dynamically modulated as the fly integrates external threat or safety cues, and artificially increasing pulse frequency leads to freezing breaks, indicating a causal role in the decision to move. Through the identification of a new Drosophila cardiac organ, this study provides a window into the multiple states which can underlie freezing behaviour, and the physiological changes which the body undergoes to ready the animal to move.

neuroscience↗

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↗

Threat induces changes in cardiac activity and metabolism negatively impacting survival in flies

Adjusting to a dynamic environment involves fast changes in the bodys internal state, characterized by coordinated alterations in brain activity, physiological and motor responses. Threat-induced defensive states are a classic example of coordinated adjustment of bodily responses, being cardiac regulation one of the best characterized in vertebrates. A great deal is known regarding the neural basis of invertebrate defensive behaviours, mainly in Drosophila melanogaster. However, whether physiological changes accompany these remains unknown. Here, we set out to describe the internal bodily state of fruit flies upon an inescapable threat and found cardiac acceleration during running and deceleration during freezing. In addition, we found that freezing leads to increased cardiac pumping from the abdomen towards the head-thorax, suggesting mobilization of energy resources. Concordantly, threat-triggered freezing reduces sugar levels in the hemolymph and renders flies less resistant to starvation. The cardiac responses observed during freezing were absent during spontaneous immobility, underscoring the active nature of freezing response. Finally, we show that baseline cardiac activity predicts the amount of freezing upon threat. This work reveals a remarkable similarity with the cardiac responses of vertebrates, suggesting an evolutionarily convergent defensive state in flies. Our findings are at odds with the widespread view that cardiac deceleration while freezing has first evolved in vertebrates and that it is energy sparing. Investigating the physiological changes coupled to defensive behaviours in the fruit fly has revealed that freezing is costly, yet accompanied by cardiac deceleration, and points to heart activity as a key modulator of defensive behaviours.

neuroscience↗

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↗

A new thalamo-cortical-amygdala circuit is involved in processing a natural auditory alarm cue

Animals use auditory cues generated by defensive responses of others to detect impending danger. Here we identify a neural circuit in rats involved in the detection of one such auditory cue, the cessation of movement-evoked sound resulting from freezing. This circuit comprises the dorsal sub-nucleus of the medial geniculate body (MGD) and downstream areas, the ventral area of the auditory cortex (VA) and the lateral amygdala (LA). This study suggests a role for the auditory offset pathway in processing a natural sound cue of threat.

neuroscience↗

Safety in numbers is mediated by motion cues and depends on lobula columnar neurons in Drosophila melanogaster

Living in a group allows individuals to decrease their defenses enabling other beneficial behaviors such as foraging. The detection of a threat through social cues is widely reported, however the safety cues that guide animals to break away from a defensive behavior and resume alternate activities remain elusive. Here we show that fruit flies displayed a graded decrease in freezing behavior, triggered by an inescapable threat, with increasing group sizes. Furthermore, flies used the cessation of movement of other flies as a cue of threat and its resumption as a cue of safety. Finally, we found that lobula columnar neurons, LC11, mediate the propensity for freezing flies to resume moving in response to the movement of others. By identifying visual motion cues, and the neurons involved in their processing, as the basis of a social safety cue this study brings new insights into the neuronal basis of safety in numbers.

neuroscience↗

Speed dependent descending control of innate freezing behavior in Drosophila melanogaster

SummaryThe most fundamental choice an animal has to make when it detects a predator, or other threats, is whether to freeze, reducing its chances of being noticed, or to flee to safety. Here we show that Drosophila melanogaster exposed to looming stimuli in a confined arena either froze or fled. The probability of freezing versus fleeing was modulated by the flys walking speed at the time of threat, demonstrating that freeze/flee decisions were context dependent. We describe a pair of descending neurons crucially implicated in freezing. Genetic silencing of P9 descending neurons disrupted freezing yet did not prevent fleeing. Optogenetic activation of both P9 neurons induced running and freezing in a state-dependent manner. Our findings establish walking speed as a key factor in defensive response choices and reveal a pair of descending neurons as a critical component in the circuitry mediating selection and execution of freezing or fleeing behaviors.

neuroscience↗