Local inhibitory neurons control the timing of neural activity in many
Local inhibitory neurons control the timing of neural activity in many circuits. fluctuations. We found a continuous spectrum of preferred stimulation timescales among LNs, as well as a continuum of ONCOFF behavior. Using whole-cell recordings, we show that the timing of an LNs 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 1408064-71-0 the dynamics of activity in a large population of inhibitory interneurons in the first brain relay of the fruit fly olfactory system. Because odor 1408064-71-0 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. antennal lobe, inhibitory interneurons, intrinsic conductances, network dynamics, olfaction, synaptic dynamics Introduction One role of inhibitory interneurons is to control the timing of neural activity (Klausberger and Somogyi, 2008; Kerlin et al., 2010; Isaacson and Scanziani, 2011). Different interneurons in the same brain region can be recruited at different times during the same sensory or behavioral event (Lapray et al., 2012; Kvitsiani et al., 2013). Interneurons recruited at different times may have different effects on the network (Royer et al., 2012; Fukunaga et al., 2014). Inhibition is thus mediated by a constantly shifting ensemble of cells, and the timing of activity across the interneuron population is likely to be central to the 1408064-71-0 function of these cells. What mechanisms cause different interneurons to be recruited at different times? Interneurons in the same brain region can receive synaptic currents with different dynamics (Reyes et al., 1998; Glickfeld and Scanziani, 2006; Savanthrapadian et al., 2014). Even with Rabbit Polyclonal to GRM7 a uniform pattern of current injection, interneurons can also exhibit diverse temporal patterns of spiking (Freund and Buzski, 1996; Markram et al., 2004; Tepper et al., 2010). Thus, both circuit and cellular mechanisms likely play a role. However, it has been challenging to link such mechanisms with activity. The antennal lobe provides a simple model for investigating the dynamics and mechanisms of interneuron population activity. This circuit contains 150 principal neurons and 200 local neurons (LNs; Stocker et al., 1990; Chou et al., 2010). The antennal lobe is the first brain relay of the olfactory system, and it shares the basic organization of the vertebrate olfactory bulb. Importantly, studies of interneurons and inhibition in the antennal lobe have presaged subsequent findings in vertebrates (Hong and Wilson, 2013; Uchida et al., 2013; Zhu et al., 2013; Banerjee et al., 2015). Most individual LNs in the antennal lobe are broadly responsive to most odors, likely because they receive input from a broad group of excitatory neurons (Okada et al., 2009; Chou et al., 2010; Seki et al., 2010). Functional diversity in the LN population lies not primarily in their selectivity for odor identity, but in the dynamics of their odor responses. Different LNs respond to the same stimulus with different temporal patterns of spikes, and the response of a given LN tends to follow a similar time course, regardless of the chemical identity of the odor (Chou et al., 2010). The finding that LNs respond with different dynamics suggests that LNs might have different preferred stimulus timescales. The issue of stimulus timescales is particularly relevant in olfaction because odors tend to form filamentous plumes. From the perspective of an observer at one point in a plume, these filaments appear as temporal fluctuations at a wide variety of timescales (Murlis et al., 1992; Celani et al., 2014). However, LN responses to fluctuating stimuli have not been investigated systematically. In this study, we investigate the timing of activity in the LN population, and the mechanisms that shape it. We.