Diverse memory paradigms in Drosophila reveal diverse neural mechanisms

Abstract

In this review, we aggregated the different types of learning and memory paradigms developed in adult Drosophila and attempted to assess the similarities and differences in the neural mechanisms supporting diverse types of memory. The simplest association memory assays are conditioning paradigms (olfactory, visual, and gustatory). A great deal of work has been done on these memories, revealing hundreds of genes and neural circuits supporting this memory. Variations of conditioning assays (reversal learning, trace conditioning, latent inhibition, and extinction) also reveal interesting memory mechanisms, whereas mechanisms supporting spatial memory (thermal maze, orientation memory, and heat box) and the conditioned suppression of innate behaviors (phototaxis, negative geotaxis, anemotaxis, and locomotion) remain largely unexplored. In recent years, there has been an increased interest in multisensory and multicomponent memories (context-dependent and cross-modal memory) and higher-order memory (sensory preconditioning and second-order conditioning). Some of this work has revealed how the intricate mushroom body (MB) neural circuitry can support more complex memories. Finally, the most complex memories are arguably those involving social memory: courtship conditioning and social learning (mate-copying and egg-laying behaviors). Currently, very little is known about the mechanisms supporting social memories. Overall, the MBs are important for association memories of multiple sensory modalities and multisensory integration, whereas the central complex is important for place, orientation, and navigation memories. Interestingly, several different types of memory appear to use similar or variants of the olfactory conditioning neural circuitry, which are repurposed in different ways.

Figure 1.

A variety of different stimuli can be used during aversive and appetitive classical conditioning paradigms. The typical training phase consists of subjecting the fly to a conditioned stimulus (CS) paired with an unconditioned stimulus (US; becoming the CS⁺), followed by a second CS without the US (becoming the CS⁻). In some paradigms, the CS⁻ precedes the CS⁺. The testing phase typically assesses the fly's avoidance or attraction to the CS⁺ compared with CS⁻.

Figure 2.

Courtship and social learning paradigms. (A) In courtship conditioning paradigms, male flies are conditioned to have their courtship advances rejected by a mated or immature female, reducing their subsequent courtship attempts with other females. (B) During mate-copying, an observer female will prefer to mate with a green-colored male (panel i) or with an unhealthy male if they previously observed a demonstrator female mating with them (panel ii). (C) Social learning of egg-laying preference information is transmitted from the demonstrator to the observer to lay eggs at sites preferred by other mated demonstrator females (panel i) or to reduce egg laying due to the presence of parasitoid wasps (panel ii).

Figure 3.

Drosophila learning and memory paradigms and their known neuroanatomical associations. Drosophila learning and memory paradigms investigated thus far are generally dependent on the MB structure or central complex structures. The brain structures necessary for several types of memory are not yet known.