Discrete Serotonin Systems Mediate Memory Enhancement and Escape Latencies after Unpredicted Aversive Experience in Drosophila Place Memory

Abstract

Feedback mechanisms in operant learning are critical for animals to increase reward or reduce punishment. However, not all conditions have a behavior that can readily resolve an event. Animals must then try out different behaviors to better their situation through outcome learning. This form of learning allows for novel solutions and with positive experience can lead to unexpected behavioral routines. Learned helplessness, as a type of outcome learning, manifests in part as increases in escape latency in the face of repeated unpredicted shocks. Little is known about the mechanisms of outcome learning. When fruit fly Drosophila melanogaster are exposed to unpredicted high temperatures in a place learning paradigm, flies both increase escape latencies and have a higher memory when given control of a place/temperature contingency. Here we describe discrete serotonin neuronal circuits that mediate aversive reinforcement, escape latencies, and memory levels after place learning in the presence and absence of unexpected aversive events. The results show that two features of learned helplessness depend on the same modulatory system as aversive reinforcement. Moreover, changes in aversive reinforcement and escape latency depend on local neural circuit modulation, while memory enhancement requires larger modulation of multiple behavioral control circuits.

Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster

“…There is a growing appreciation for the complexity of learning and memory and the need to study these traits in realistic settings 4,116 . Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory 54,87,117,118 . In addition, mapping studies in humans are beginning to uncover the natural genetic variants influencing learning and memory 25,119…”

A biphasic locomotor response to acute unsignaled high temperature exposure in Drosophila

“…In rats, long term (3 weeks to 3 months) exposure to different stressors such as water deprivation, food deprivation or exposure to cold temperatures produces changes in sleep and anhedonic behavior [ 2 ]. Moreover, in insects like Drosophila , extended exposure to aversive heat, electric shock, or vibration impacts multiple behaviors including changes in motivated behaviors like learning, locomotion, and courtship [ 3 – 6 ].…”

“…Moreover, in heat-box and shock-box paradigms, flies will continue to walk back and forth in a dark, narrow chamber for several hours [ 5 , 6 , 14 ]. Exposure to aversive high temperatures or electric shocks over several minutes reduces walking activity and increases escape latencies [ 3 – 6 ]. What is less understood is the acute locomotor response to aversive temperatures or electric shocks.…”

Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster

“…4,116 Recently there has been a shift from investigating single genes to identifying the sets of neurons and circuits involved in learning and memory. 54,87,117,118 In addition, mapping studies in humans are beginning to uncover the natural genetic variants influencing learning and memory. 25,119 Although it is still early, the challenges associated with studying human learning and memory suggest that a complete picture of how a genome can support fundamental learning and memory mechanisms remains in the future.…”