Persistent activity in a recurrent circuit underlies courtship memory in Drosophila

Abstract

Recurrent connections are thought to be a common feature of the neural circuits that encode memories, but how memories are laid down in such circuits is not fully understood. Here we present evidence that courtship memory in Drosophila relies on the recurrent circuit between mushroom body gamma (MBγ), M6 output, and aSP13 dopaminergic neurons. We demonstrate persistent neuronal activity of aSP13 neurons and show that it transiently potentiates synaptic transmission from MBγ>M6 neurons. M6 neurons in turn provide input to aSP13 neurons, prolonging potentiation of MBγ>M6 synapses over time periods that match short-term memory. These data support a model in which persistent aSP13 activity within a recurrent circuit lays the foundation for a short-term memory.

Social behavior and aging: A fly model

“…222 This phenomenon, called courtship conditioning, can be utilized for the study of learning and memory in various contexts. [224][225][226] However, courtship memory also depends on the circadian rhythm related gene period that is expressed in a cAMP-responsive transcription factor, CREB, dependent fashion by fan-shaped body neurons. Surprisingly, using this paradigm, long-term courtship memory has been reported to last up to 9 days.…”

“…224 Similar to other olfactory-based memory tasks, courtship memory has been shown to depend on the mushroom body region of the brain, where cVA perception is modulated by DA signaling in response to past experience. [224][225][226] However, courtship memory also depends on the circadian rhythm related gene period that is expressed in a cAMP-responsive transcription factor, CREB, dependent fashion by fan-shaped body neurons. 227 To date, few studies have assessed age-related changes in response to courtship conditioning, and the results are contradictory.…”

Multilevel feedback architecture for adaptive regulation of learning in the insect brain

“…Modulatory neurons (e.g. dopaminergic, DAN) are key components of higher-order circuits for adaptive behavioral control, such as the vertebrate basal ganglia or the insect mushroom body (MB), and they provide teaching signals that drive memory formation and updating 12,14,21,24,25,49,58,66 . Here, we provide the first synaptic-resolution connectivity map of a recurrent neural network that regulates the activity of all modulatory neurons in a higher-order learning center, the Drosophila larval MB ( Fig.…”

“…However, the extent to which learning in a specific compartment is regulated by the output from its own compartment or from other compartments is still unclear. A few direct anatomical connections from MBONs to modulatory neurons have been identified 13,14,[45][46][47][48][49]53,54 , but possible indirect connections via intermediate feedback neurons have not been investigated. In total, despite a good understanding of the structure and function of the core components of the MB 14,47,48,58 , the circuits presynaptic to modulatory neurons that regulate their activity have re-mained largely uncharacterized, in both adult and larval Drosophila.…”

Learning with reward prediction errors in a model of the Drosophila mushroom body

“…To date, there are only indirect lines of evidence for RPE signals in MB DANs. DAN activity is modulated by feedforward reward signals, but some DANs also receive excitatory feedback from MBONs (12)(13)(14)(15), and it is likely this extends to all MBONs whose axons are proximal to DAN dendrites (16). MBON activity is, in turn, modulated by DANs via plasticity at KC→MBON synapses (10; 17; 18).…”