Behavioral Responses to a Repetitive Visual Threat Stimulus Express a Persistent State of Defensive Arousal in Drosophila

Abstract

Summary The neural circuit mechanisms underlying emotion states remain poorly understood. Drosophila offers powerful genetic approaches for dissecting neural circuit function, but whether flies exhibit emotion-like behaviors has not been clear. We recently proposed that model organisms may express internal states displaying “emotion primitives,” which are general characteristics common to different emotions, rather than specific anthropomorphic emotions such as “fear” or “anxiety”. These emotion primitives include scalability, persistence, valence and generalization to multiple contexts. Here we have applied this approach to determine whether flies' defensive responses to shadows are purely reflexive, or may express underlying emotion states. We describe a new behavioral assay in which flies confined in an enclosed arena are repeatedly exposed to an overhead translational shadow. Repetitive shadows promoted graded (scalable) and persistent increases in locomotor velocity and hopping, and occasional freezing. The shadow also dispersed feeding flies from a food resource, suggesting both negative valence and context generalization. Strikingly, there was a significant delay before the flies returned to the food following shadow-induced dispersal, suggestive of a slowly decaying internal defensive state. The length of this delay was increased when more shadows were delivered for initial dispersal. These responses can be mathematically modeled by assuming an internal state that behaves as a leaky integrator of shadow exposure. Our results suggest that flies' responses to repetitive shadow stimuli express an internal state exhibiting canonical emotion primitives, possibly analogous to “fear” in mammals. The mechanistic basis of this state can now be investigated in a genetically tractable insect species.

Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans

“…This arrangement suggests that information can be integrated across the circuit (36 We see parallels between our observations and a Drosophila study showing that repeated presentation of an aversive shadow cue leads to a persistent change in behavioral state that scales with the number and frequency of the presentations (55,56). Our findings are also reminiscent of "latent modulation" in the feeding network of Aplysia, where the history of activation in some circuit elements has a lasting effect on subsequent responses, most likely by changing neuronal excitability through peptidergic modulation (57,58).…”

Preemptive Stimulation of AgRP Neurons in Fed Mice Enables Conditioned Food Seeking under Threat

“…For example, the efficacy of a mounting sleep drive is mitigated by sustained, stressor-induced activation of arousal circuitry [21]. Similarly, placement of mice into our threat-containing arena in a fed state may permit induction of arena-induced, sustained activation of stress-related circuits, analogous to the persistent state of defensive arousal observed in a recent study in Drosophila [23]. As with sleep drive, a mounting food-seeking drive may not be able to overcome this stressor-induced defensive state once it is initiated.…”

“…In contrast, entering the arena with AgRP neuron stimulation already underway may act to prevent such a defensive state from arising, potentially through a combination of reduced contextual fear [11] and hunger-induced analgesia [24]. Work in invertebrate systems has begun to elucidate the circuit mechanisms underlying such competitive interactions [25–26], and behavioral paradigms have recently been developed to investigate these interactions in Drosophila [23]. The paradigm we introduce here provides a similar starting point for probing such circuit mechanisms in an experimentally tractable mammalian model system.…”

Affordances and the normativity of emotions

“…Being alive, mortal, and vulnerable implies the possibility of being in danger. Accordingly, we find homologous forms of fear in animals such as zebrafish (Kalueff et al 2012) and fruitflies (Gibson et al 2015) that enables them to avoid dangerous situations. The same is true for disgust (Kelly 2011).…”