Coincident postsynaptic activity gates presynaptic dopamine release to induce plasticity in Drosophila mushroom bodies

Abstract

Simultaneous stimulation of the antennal lobes (ALs) and the ascending fibers of the ventral nerve cord (AFV), two sensory inputs to the mushroom bodies (MBs), induces long-term enhancement (LTE) of subsequent AL-evoked MB responses. LTE induction requires activation of at least three signaling pathways to the MBs, mediated by nicotinic acetylcholine receptors (nAChRs), NMDA receptors (NRs), and D1 dopamine receptors (D1Rs). Here, we demonstrate that inputs from the AL are transmitted to the MBs through nAChRs, and inputs from the AFV are transmitted by NRs. Dopamine signaling occurs downstream of both nAChR and NR activation, and requires simultaneous stimulation of both pathways. Dopamine release requires the activity of the rutabaga adenylyl cyclase in postsynaptic MB neurons, and release is restricted to MB neurons that receive coincident stimulation. Our results indicate that postsynaptic activity can gate presynaptic dopamine release to regulate plasticity.DOI: http://dx.doi.org/10.7554/eLife.21076.001

Recurrent loops: Incorporating prediction error and semantic/episodic theories into Drosophila associative memory models

“…Since dopaminergic neurons innervate the MBs bilaterally, this indicates that there must be a mechanism that restricts dopaminergic release to activated postsynaptic cells. Ueno et al propose that Kenyon cell that has been activated by an odor send a retrograde signal to pre‐synaptic dopaminergic terminals to gate dopamine release . Thus, release requires the convergence of two signals, first, activation of dopaminergic cells from the episodic trace, and second, a gating signal generated by odor‐activated post‐synaptic Kenyon cells.…”

“…Co‐incident stimulation of the AFV and the AL induces long‐term enhancement (LTE) of AL‐dependent MB Ca 2+ responses. (Modified from Ueno et al, 2017)…”

“…In dissected brains, signal transmission from the ALs to the MBs is mediated by cholinergic receptors, a result consistent with previous in vivo results. Transmission from the AFV to the MBs also does not require dopaminergic receptors in the MBs, and instead requires N‐methyl‐D‐aspartate (NMDA)‐type glutamate receptors . Dopamine is released onto the MBs at a step after coincident sensory input to the MBs and is required for plasticity.…”

“…Ex vivo studies from Ueno et al suggest that dopamine release is limited to Kenyon cells that have been activated by odor stimuli. If the antennal lobe on only one side of the brain is electrically stimulated (mimicking odor stimulation) while concurrently pharmacologically activating glutamate receptors bilaterally (mimicking shock application), dopamine is released only onto the MBs ipsilateral to the activated antennal lobe . Since dopaminergic neurons innervate the MBs bilaterally, this indicates that there must be a mechanism that restricts dopaminergic release to activated postsynaptic cells.…”

Synaptic depression induced by postsynaptic cAMP production in the Drosophila mushroom body calyx

“…Brains were prepared for imaging analysis as previously described with minor modifications (Ueno et al . , ; Naganos et al . ).…”