Functional integration of a serotonergic neuron in the Drosophila antennal lobe

Abstract

Serotonin plays a critical role in regulating many behaviors that rely on olfaction and recently there has been great effort in determining how this molecule functions in vivo. However, it remains unknown how serotonergic neurons that innervate the first olfactory relay respond to odor stimulation and how they integrate synaptically into local circuits. We examined the sole pair of serotonergic neurons that innervates the Drosophila antennal lobe (the first olfactory relay) to characterize their physiology, connectivity, and contribution to pheromone processing. We report that nearly all odors inhibit these cells, likely through connections made reciprocally within the antennal lobe. Pharmacological and immunohistochemical analyses reveal that these neurons likely release acetylcholine in addition to serotonin and that exogenous and endogenous serotonin have opposing effects on olfactory responses. Finally, we show that activation of the entire serotonergic network, as opposed to only activation of those fibers innervating the antennal lobe, may be required for persistent serotonergic modulation of pheromone responses in the antennal lobe.DOI: http://dx.doi.org/10.7554/eLife.16836.001

Examining Monosynaptic Connections in <em>Drosophila</em> Using Tetrodotoxin Resistant Sodium Channels

“…Each color across simulation intensities corresponds to the same color in the voltage inset. This figure has been modified from Zhang and Gaudry 2016 99 .…”

“…The vertical gray bar indicates the timing of ORN stimulation. This figure has been modified from Zhang and Gaudry in 2016 9 .…”

“…The brief depolarization that remains in TTX is likely mediated by electrical gap coupling, as it not blocked by nicotinic antagonists. This figure has been modified from Zhang and Gaudry in 2016 9 .…”

“…While GRASP and its variants have been instrumental in determining functional connectivity in the Drosophila CNS, some connections may not be made visible by GRASP if the distances between pre- and postsynaptic partners is relatively large. This is particularly pertinent in the assessment of volume transmission associated with neuromodulation 9 or GABAergic inhibition 10 .…”

“…This method, called Tetrodotoxin Engineered Resistance for Probing Synapses (TERPS), works by co-expression of the tetrodotoxin (TTX)-resistant sodium channel, NaChBac, and an optogenetic activator in a presynaptic cell while recording from putative postsynaptic partners 9 . In the presence of TTX, all action potential-mediated activity is suppressed in cells other than those expressing NaChBac.…”