Essential Role of the Mushroom Body in Context-Dependent CO2 Avoidance in Drosophila

Abstract

Internal state as well as environmental conditions influence choice behavior. The neural circuits underpinning state-dependent behavior remain largely unknown. Carbon dioxide (CO2) is an important olfactory cue for many insects, including mosquitoes, flies, moths, and honeybees [1]. Concentrations of CO2 higher than 0.02% above atmospheric level trigger a strong innate avoidance in the fly Drosophila melanogaster [2, 3]. Here, we show that the mushroom body (MB), a brain center essential for olfactory associative memories [4-6] but thought to be dispensable for innate odor processing [7], is essential for CO2 avoidance behavior only in the context of starvation or in the context of a food-related odor. Consistent with this, CO2 stimulation elicits Ca(2+) influx into the MB intrinsic cells (Kenyon cells: KCs) in vivo. We identify an atypical projection neuron (bilateral ventral projection neuron, biVPN) that connects CO2 sensory input bilaterally to the MB calyx. Blocking synaptic output of the biVPN completely abolishes CO2 avoidance in food-deprived flies, but not in fed flies. These findings show that two alternative neural pathways control innate choice behavior, and they are dependent on the animal's internal state. In addition, they suggest that, during innate choice behavior, the MB serves as an integration site for internal state and olfactory input.

Compound valence is conserved in binary odor mixtures in Drosophila melanogaster

“…The MB is generally considered the brain center for odor identification and learning, while the LH has been implicated to be involved in innate behavior (de Belle and Heisenberg, 1994;Heimbeck et al, 2001;Jefferis et al, 2007). MB output has recently been described to be important for CO 2 avoidance in the context of starvation (Bräcker et al, 2013) and therefore does play a role in innate behavior under certain circumstances. However, blocking MB output during an odor discrimination task in trained flies restores innate preferences (Parnas et al, 2013), suggesting that these preferences are hard-wired in the LH circuitry.…”

Targeted manipulation of neuronal activity in behaving adult flies

“…To ensure consistency of behavioral experiments, many groups use circadian-entrained flies that are all tested at the same time of day (Vinayak et al 2013). Third, hunger influences fly behaviors such as food searching (Root et al 2011;Gruber et al 2013), innate avoidance (Bräcker et al 2013), learning (Krashes et al 2009), and locomotion (Knoppien et al 2000;Lee and Park 2004;Albin et al 2015). Furthermore, the food recipe and number of flies reared on a particular volume of food can affect behavior (Guo et al 1996).…”

Neural mechanisms of context-dependent processing of CO2 avoidance behavior in fruit flies

“…Based on a previous finding that feeding state can be integrated at the level of the mushroom body (MB) during appetitive learning and memory, 12 in our work we explored the role of the MB in feeding state-dependent CO 2 avoidance behavior 11 . The MB has been studied to a great extent for its essential role in various behaviors.…”

“…In a recent report we used CO 2 choice behavior to unravel the impact of feeding state on olfactory choice behavior and the underpinning neural circuit mechanisms 11 . First, we hypothesized that the feeding-state of the fly may modulate the representation of CO 2 in the brain, in particular in the context of feeding on ripening or rotting fruits.…”

“…In support of these behavioral experiments, using in vivo calcium imaging experiments we showed that CO 2 stimulation elicits a calcium response in KCs in a concentration-dependent manner. Thus, the MB is required for processing innate olfactory behavior exclusively in the context of internal state or additional external stimuli 11 . By using GFP-photoconversion experiments, and an extensive search of a GAL4-database, we identified a bilateral ventral projection neuron (biVPN) that connects the V-glomerulus to the higher brain centers.…”