Odor-Induced Multi-Level Inhibitory Maps inDrosophila

Abstract

Optical imaging of intracellular Ca 2ϩ influx as a correlate of neuronal excitation represents a standard technique for visualizing spatiotemporal activity of neuronal networks. However, the information-processing properties of single neurons and neuronal circuits likewise involve inhibition of neuronal membrane potential. Here, we report spatially resolved optical imaging of odor-evoked inhibitory patterns in the olfactory circuitry of Drosophila using a genetically encoded fluorescent Clsensor. In combination with the excitatory component reflected by intracellular Ca 2ϩ dynamics, we present a comprehensive functional map of both odor-evoked neuronal activation and inhibition at different levels of olfactory processing. We demonstrate that odor-evoked inhibition carried by Clinflux is present both in sensory neurons and second-order projection neurons (PNs), and is characterized by stereotypic, odor-specific patterns. Cl --mediated inhibition features distinct dynamics in different neuronal populations. Our data support a dual role of inhibitory neurons in the olfactory system: global gain control across the neuronal circuitry and glomerulus-specific inhibition to enhance neuronal information processing.

Experience-dependent plasticity modulates ongoing activity in the antennal lobe and enhances odor representations

“…A potential mechanism for such plasticity may rely on a gradual recruitment of inhibitory local interneurons (LNs) of the antennal lobe. A large fraction of LNs are inhibitory ( Berck et al., 2016 ; Chou et al., 2010 ; Nagel et al., 2015 ; Olsen et al., 2010 ; Sachse et al., 2007 ), regulating the activity of projection neurons ( Franco et al., 2017 ; Grabe et al, 2020 ; Wilson and Laurent, 2005 ) and olfactory receptor neuron terminals ( Olsen and Wilson, 2008 ; Root et al., 2008 ). Thus, it is likely that repeated odor exposure gradually increases the activity of inhibitory LNs, leading to accumulating levels of the inhibitory neurotransmitter gamma-aminobutyric acid in the antennal lobe.…”

Experience-dependent plasticity modulates ongoing activity in the antennal lobe and enhances odor representations

“…A potential mechanism for such plasticity may rely on a gradual recruitment of the inhibitory local interneurons of the antennal lobe. A relatively large fraction of antennal lobe local interneurons (LNs) are inhibitory (Berck et al, 2016; Chou et al, 2010; Nagel et al, 2015; Olsen et al, 2010; Sachse et al, 2007), regulating the activity of both projection neurons (Franco et al, 2017; Grabe et al, 2020; Wilson and Laurent, 2005) and olfactory receptor neuron terminals (Olsen and Wilson, 2008; Root et al, 2008). Thus, it is likely that repeated odor exposure gradually increases the activity of inhibitory LNs, leading to accumulating levels of the inhibitory neurotransmitter GABA release in the antennal lobe.…”

Odor response adaptation in Drosophila—a continuous individualization process

“…1c, Olsen and Wilson 2008;Wilson and Laurent 2005). GABAergic LNs form synapses with OSNs (Olsen and Wilson 2008;Root et al 2008;Wilson and Laurent 2005), and the various OSN classes differ in GABA sensitivity (Grabe et al 2020;Hong and Wilson 2015). The size of the GABA response relates to the size of the odor response, with larger responses acting to dampen extreme OSN/PN activity (Grabe et al 2020;Olsen and Wilson 2008).…”

“…GABAergic LNs form synapses with OSNs (Olsen and Wilson 2008;Root et al 2008;Wilson and Laurent 2005), and the various OSN classes differ in GABA sensitivity (Grabe et al 2020;Hong and Wilson 2015). The size of the GABA response relates to the size of the odor response, with larger responses acting to dampen extreme OSN/PN activity (Grabe et al 2020;Olsen and Wilson 2008). This suppression results in a gain control mechanism that increases the dynamic range of information transmission (Olsen and Wilson 2008;Root et al 2008;Wilson and Laurent 2005).…”

“…Large-scale transduction studies have been limited by the array of mixed OSN classes on the antennal surface combined with the low spatial resolution of imaging techniques. Nevertheless, tour de force studies have recently pushed back at these limitations (Grabe et al 2020;Seki et al 2017). Ultimately, future studies must provide the necessary spatial resolution to observe the filtering that takes place between OSN classes at all stages of adaptation.…”