A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Abstract

Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly's learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly's ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β'1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β'1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β'2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit.

Innate and learned odor-guided behaviors utilize distinct molecular signaling pathways in a shared dopaminergic circuit

“… 12 , 19 – 21 , 40 – 42 , 59 – 61 Interestingly, the majority of reports define a role for MBns in innate behavioral responses to food-related odors. 12 , 18 – 20 , 40 – 42 Our results, using more general, non-food odors, puts the hypothesis that MBn regulates innate behavior on more solid ground. Importantly, we found that MB dDA1 is required for state-dependent behavior to general odors ( Figure 5C ).…”

“… 17 However, recent discoveries have revealed that the Drosophila mushroom body (MB) is required for innate olfactory behavior as well as its historically defined role in learning. 12 , 18 – 20 The current hypothesis states that both behaviors are driven by cholinergic connections between MB neurons (MBns) and downstream MB-output neurons (MBONs) 21 and that innervating dopaminergic neurons (DANs) modulate this connection in response to learning and internal state. It is unknown how dopaminergic input to the MB controls these two discrete behaviors.…”

Independent insulin signaling modulators govern hot avoidance under different feeding states

“…It has been shown that MBON-α′3 forms a suppressed short-lived memory trace following aversive olfactory conditioning, whose activity is required for the 15-min memory [ 56 ]. In addition, MBON-β′1 activity is critical for polyamine odor preference and mating behaviors in female flies [ 57 ]. Our results showed the physiological roles of MBON-α′3 and MBON-β′1, which are responsive to hot stimuli and regulate HAB execution in Drosophila ( Fig 7 ).…”

Ants prefer the option they are trained to first

“…An alternative explanation for our findings is that, after their initial encounter with the food, the ants are less hungry, and thus food becomes less of a motivation to learn in subsequent visits. Such state-dependent learning has been demonstrated in insects in both foraging ( Pompilio et al, 2006 ) and mating ( Boehm et al, 2022 ) contexts, and has been implicated in the driving of preference in ants ( Czaczkes et al, 2018 ). While ants continue to make many tens of foraging visits if allowed, demonstrating a consistent and high motivation ( Oberhauser et al, 2020a ), the first encounter with a food source after 4 days of food deprivation is likely to be especially salient.…”