Reinforcement pre-exposure enhances spatial memory formation in Drosophila

Abstract

Apparently unpaired exposure to appetitive or aversive stimuli can suppress or enhance later associative learning. While the suppressive effect has been found in both vertebrate and invertebrate animals, it is not clear if the enhancing effect is restricted to the vertebrates. Additionally, whether Drosophila associative learning can be influenced in either direction is open. To address these questions, we examined the effects of pre-exposing flies to a high temperature negative reinforcer in the heat-box place-learning paradigm. We found that pre-exposing flies to an unavoidable high temperature enhanced later associative conditioning that uses mild increases in temperature. This enhancement lasts at least 20 min, does not depend on changes in the straightforward avoidance behavior of a high temperature source, and is independent of the antennal thermosensor. We thus provide an example of enhanced associative learning after unpaired exposure to a typical reinforcer in an invertebrate animal, suggesting the conservation of this component of learning.

Lack of prediction for high-temperature exposures enhances Drosophila place learning

“…In the first experiment, we conditioned master and yoked flies in five 6-min training sessions with the 24/41°C contingency. We chose these conditions because we know that, in straightforward experiments, 3min of high-temperature exposure induces a strong pre-exposure effect and 30min of training should lead to approximately 3min of exposure to high temperatures (Diegelmann et al, 2006;Sitaraman et al, 2007). Examination of the behavior of two individual flies revealed coherent avoidance behavior in only the master fly during the yoking phase of the experiment.…”

“…This enhancement is evident in a test phase when flies are conditioned with a relatively weak reinforcing temperature. The high-temperature pre-exposure does not alter the ability of flies to sense and avoid high temperatures, suggesting that the pre-exposure effect alters nervous system physiology in a non-peripheral fashion (Sitaraman et al, 2007).…”

“…The training phase is followed by a test phase in which the chamber is maintained at 24°C, and flies typically continue to avoid the side previously associated with high temperature. Interestingly, flies pre-exposed to an inescapable 41°C environment before conditioning have enhanced memory levels (Sitaraman et al, 2007). This enhancement is evident in a test phase when flies are conditioned with a relatively weak reinforcing temperature.…”

“…Moreover, unpredictable aversive stimuli have induced a higher degree of anxiety compared with predictable stimuli in experiments with human subjects (Grillon et al, 2004). Thus far, the only clear evidence that reinforcer preexposure enhances later performance in associative conditioning in an invertebrate animal comes from Drosophila, where pre-exposure to aversive high temperatures enhances later place learning (Sitaraman et al, 2007). Thus, it seems that the perception of the unpredictability of aversive stimuli can have lasting effects on physiology and behavior and is a property found in widely different animal species; this perception can influence memory formation.…”

“…Pre-exposure to high temperature enhances spatial memory formation in an operant learning paradigm called the heat box (Sitaraman et al, 2007). In Drosophila place learning, a fly is free to roam inside a narrow but relatively long chamber.…”