Context generalization in Drosophila visual learning requires the mushroom bodies

Abstract

The world is permanently changing. Laboratory experiments on learning and memory normally minimize this feature of reality, keeping all conditions except the conditioned and unconditioned stimuli as constant as possible. In the real world, however, animals need to extract from the universe of sensory signals the actual predictors of salient events by separating them from non-predictive stimuli (context). In principle, this can be achieved if only those sensory inputs that resemble the reinforcer in their temporal structure are taken as predictors. Here we study visual learning in the fly Drosophila melanogaster, using a flight simulator, and show that memory retrieval is, indeed, partially context-independent. Moreover, we show that the mushroom bodies, which are required for olfactory but not visual or tactile learning, effectively support context generalization. In visual learning in Drosophila, it appears that a facilitating effect of context cues for memory retrieval is the default state, whereas making recall context-independent requires additional processing.

Mental retardation genes in drosophila: New approaches to understanding and treating developmental brain disorders

“…For example, flies learn to avoid an odor that has been paired with electric shock (classical olfactory conditioning) or a spatial location where they were exposed to a noxious heat stimulus (operant place learning). When the task is made more complex by the addition of irrelevant sensory stimuli, flies can still learn the relevant predictive cue [Liu et al, 1999]. In an even more complex form of behavioral plasticity, when the sexual advances of a male fruit fly are rebuffed by a nonreceptive female, the male responds with a prolonged reduction in his courtship activity (courtship conditioning) [Tompkins et al, 1983;Mehren et al, 2004].…”

Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach

“…In addition to playing a critical role in olfactory learning (Erber et al, 1980;de Belle and Heisenberg, 1994;Krashes et al, 2007), MBs are also implicated in mediating or modulating some complex adaptive behaviors including visual context generalization (Liu et al, 1999), visual place learning (Mizunami et al, 1998d), choice behavior (Tang and Guo, 2001), courtship conditioning (McBride et al, 1999), and sleep (Joiner et al, 2006;Pitman et al, 2006).…”

Dissociation of visual associative and motor learning in Drosophila at the flight simulator

“…It is now clear that in olfactory classical conditioning (Tully and Quinn, 1985) the CS-US association mostly occurs within mushroom bodies (MBs) (Dubnau et al, 2001;McGuire et al, 2001). With the operant conditioning paradigm, the MBs were demonstrated to be dispensable for the visual associative learning (Wolf et al, 1998) but were necessary for some cognition-like functions (Liu et al, 1999;Tang and Guo, 2001). However, further cellular or molecular evidences related to the visual associative learning and related functions remain unknown.…”

“…In this paradigm, the fly was trained to discriminate the flight direction with reference to two kinds of visual patterns where one pattern type was associated with heat punishment by this paradigm, such as context generalization (Liu et al, 1999), visual selective attention (Wu et al, 2000), and choice behaviour facing competing alternatives (Tang and Guo, 2001).…”