Mechanisms Underlying Population Response Dynamics in Inhibitory Interneurons of the Drosophila Antennal Lobe

Local inhibitory neurons control the timing of neural activity in many circuits. To understand how inhibition controls timing, it is important to understand the dynamics of activity in populations of local inhibitory interneurons, as well as the mechanisms that underlie these dynamics. Here we describe the in vivo response dynamics of a large population of inhibitory local neurons (LNs) in the Drosophila melanogaster antennal lobe, the analog of the vertebrate olfactory bulb, and we dissect the network and intrinsic mechanisms that give rise to these dynamics. Some LNs respond to odor onsets (“ON” cells) and others to offsets (“OFF” cells), whereas still others respond at both times. Moreover, different LNs signal odor concentration fluctuations on different timescales. Some respond rapidly, and can track rapid concentration fluctuations. Others respond slowly, and are best at tracking slow fluctuations. We found a continuous spectrum of preferred stimulation timescales among LNs, as well as a continuum of ON–OFF behavior. Using in vivo whole-cell recordings, we show that the timing of an LN′s response (ON vs OFF) can be predicted from the interplay of excitatory and inhibitory synaptic currents that it receives. Meanwhile, the preferred timescale of an LN is related to its intrinsic properties. These results illustrate how a population of inhibitory interneurons can collectively encode bidirectional changes in stimulus intensity on multiple timescales, and how this can arise via an interaction between synaptic and intrinsic mechanisms. SIGNIFICANCE STATEMENT Most neural circuits contain diverse populations of inhibitory interneurons. The way inhibition shapes network activity will depend on the spiking dynamics of the interneuron population. Here we describe the dynamics of activity in a large population of inhibitory interneurons in the first brain relay of the fruit fly olfactory system. Because odor plumes fluctuate on multiple timescales, the drive to this circuit can vary over a range of frequencies. We show how synaptic and cellular mechanisms interact to recruit different interneurons at different times, and in response to different temporal features of odor stimuli. As a result, inhibition is recruited over a range of conditions, and there is the potential to tune the timing of inhibition as the environment changes.