Dopamine modulates the optomotor response to unreliable visual stimuli in Drosophila melanogaster

Abstract

State‐dependent modulation of sensory systems has been studied in many organisms and is possibly mediated through neuromodulators such as monoamine neurotransmitters. Among these, dopamine is involved in many aspects of animal behaviour, including movement control, attention, motivation and cognition. However, the precise neural mechanism underlying dopaminergic modulation of behaviour induced by sensory stimuli remains poorly understood. Here, we used Drosophila melanogaster to show that dopamine can modulate the optomotor response to moving visual stimuli including noise. The optomotor response is the head‐turning response to moving objects, which is observed in most sight‐reliant animals including mammals and insects. First, the effects of the dopamine system on the optomotor response were investigated in mutant flies deficient in dopamine receptors D1R1 or D1R2, which are involved in the modulation of sleep‐arousal in flies. We examined the optomotor response in D1R1 knockout (D1R1 KO) and D1R2 knockout (D1R2 KO) flies and found that it was not affected in D1R1 KO flies; however, it was significantly reduced in D1R2 KO flies compared with the wild type. Using cell‐type‐specific expression of an RNA interference construct of D1R2, we identified the fan‐shaped body, a part of the central complex, responsible for dopamine‐mediated modulation of the optomotor response. In particular, pontine cells in the fan‐shaped body seemed important in the modulation of the optomotor response, and their neural activity was required for the optomotor response. These results suggest a novel role of the central complex in the modulation of a behaviour based on the processing of sensory stimulations.

A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…Previous experimental work has implicated FB circuits in a variety of behaviors that require directed movements, including operant visual learning ( Liu et al, 2006 ), obstacle avoidance ( Harley and Ritzmann, 2010 ), nociceptive avoidance ( Hu et al, 2018 ), and head optomotor responses ( Akiba et al, 2020 ). Further, recent physiological recordings have demonstrated that PB-FB columnar neurons convey the head direction representation from the left and right PB to the FB ( Shiozaki et al, 2020 ), and that, similar to the PEN neurons, PFN activity is likely modulated by self-motion inputs received in the NO ( Currier et al, 2020 ; Lu et al, 2020b ; Lyu et al, 2020 ; Shiozaki et al, 2020 ; Stone et al, 2017 ).…”

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…Previous experimental work has implicated FB circuits in a variety of behaviors that require directed movements, including operant visual learning (Liu et al, 2006), obstacle avoidance (Harley and Ritzmann, 2010), nociceptive avoidance (Hu et al, 2018), and head optomotor responses (Akiba et al, 2020). Further, recent physiological recordings have demonstrated that PB-FB columnar neurons convey the head direction representation from the left and right PB to the FB (Shiozaki et al, 2020), and that, similar to the PEN neurons, PFN activity is likely modulated by self-motion inputs received in the NO (Currier et al, 2020;Lu et al, 2020a;Lyu et al, 2020;Shiozaki et al, 2020;Stone et al, 2017).…”

Interneurons of fan-shaped body promote arousal in Drosophila

“…Based on the morphological similarities, we assumed that one of the candidates of the post-synaptic neurons of P-FN neurons is FB interneurons, also known as pontine neurons 17,18 . Among the Gal4 drivers, NP2320-Gal4 is a driver that is reported in the previous papers to show clear labeling in pontine neurons 19–22 . Figure 1b shows the morphological patterns of pontine neurons labeled with NP2320-Gal4 (Fig.…”

“…According to previous reports, pontine neurons regulate optomotor behavior and express tachykinin, a neuropeptide that regulates aggression 20,22,32 . Additionally, T1 dopamine neurons, which are upstream of pontine neurons, regulate aggression as well 33 .…”

“…Among the Gal4 drivers, NP2320-Gal4 is a driver that is reported in the previous papers to show clear labeling in pontine neurons [19][20][21][22] . Figure 1b shows the morphological patterns of pontine neurons labeled with NP2320-Gal4 (Fig.…”