Auditory circuit in the Drosophila brain

Abstract

Most animals exhibit innate auditory behaviors driven by genetically hardwired neural circuits. In Drosophila, acoustic information is relayed by Johnston organ neurons from the antenna to the antennal mechanosensory and motor center (AMMC) in the brain. Here, by using structural connectivity analysis, we identified five distinct types of auditory projection neurons (PNs) interconnecting the AMMC, inferior ventrolateral protocerebrum (IVLP), and ventrolateral protocerebrum (VLP) regions of the central brain. These auditory PNs are also functionally distinct; AMMC-B1a, AMMC-B1b, and AMMC-A2 neurons differ in their responses to sound (i.e., they are narrowly tuned or broadly tuned); one type of audioresponsive IVLP commissural PN connecting the two hemispheres is GABAergic; and one type of IVLP-VLP PN acts as a generalist responding to all tested audio frequencies. Our findings delineate an auditory processing pathway involving AMMC→IVLP→VLP in the Drosophila brain.calcium imaging | FlyCircuit | GFP reconstitution across synaptic partners | polarity A uditory systems are critical to the behavior of many insects. In Drosophila melanogaster, acoustic communication is essential for making decisions related to mate selection (1-4). During courtship, male flies flap one wing to produce a complex pattern of airborne vibrations comprising sine song and pulse song (5, 6). The pulse song enables the female to determine whether her suitor is of the same species (7). Courting males also monitor their own sounds to fine tune the courtship song (8). The courtship song is detected by auditory sensory neurons linking the Johnston organ (JO) at the second antennal segment to the antennal mechanosensory and motor center (AMMC) zones AB in the brain (9-12). It has been shown that the transient receptor potential vanilloid channels (Inactive and Nanchung) and a no mechanoreceptor potential C TRP channel expressed in JO-AB neurons are essential for normal acoustic transduction (13-16).Four different projection neurons (PNs) innervating the AMMC zones AB have been reported based on Gal4 expression patterns (12). The giant fiber neuron links AMMC zone A to the inferior ventrolateral protocerebrum (IVLP; a brain region defined by immunostaining of synaptic proteins) and thoracic ganglia; AMMC-A1 neuron connects AMMC zone A and the IVLP; AMMC-B1 neuron links AMMC zone B to the IVLP; and AMMC-B2 neurons are commissural neurons connecting AMMC zone B in both hemispheres. The intense innervations of the IVLP suggest that the IVLP functions as a second-level auditory processing center (12). More recently, stochastic labeling of 16,000 single neurons in the entire fly brain revealed that many AMMC PNs terminate at the caudoventrolateral protocerebrum (CVLP; a brain region analogous to IVLP and defined by clustered local neurons) (17), suggesting that the IVLP/CVLP region may be involved in auditory functions. However, a structural and functional map of cell-to-cell connectivity is first required to determine the direction of information flow,...

Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects

“…NTL is expressed primarily in the central interneurons that extensively innervate the ventrolateral protocerebrum (VLP), where olfactory, gustatory, auditory, and visual pathways converge (27)(28)(29)(30). Thus, we examined the role of NTL and NTL-expressing neurons in mating behavior, which requires flies to integrate and coordinate virtually all sensory modalities to execute multiple motor programs.…”

Connecting Neural Codes with Behavior in the Auditory System of Drosophila

“…Given that our knowledge of higher-order auditory neurons in the Drosophila brain is limited (Lai et al, 2012;Zhou et al, 2014), the utility of our decoder model is that it posits simple algorithms for transforming the auditory codes of AMMC/VLP neurons into behavioral responses to courtship song. We propose that an AMMC/VLP neuron is read out by two downstream neurons.…”

“…Ipsilateral/contralateral defined with respect to soma position. 2 Lai et al 2012. 3 Vaughan et al 2014 …”

“…The two major populations of sound-responsive JONs terminate in AMMC zones A and B Yorozu et al, 2009). Recent studies have mapped several of the central neurons that innervate these zones (Lai et al, 2012;Vaughan et al, 2014), and have found that most project to a nearby neuropil termed the ventrolateral protocerebrum (VLP). Projections from the VLP to other brain regions remain uncharacterized (but see Yu et al (2010)).…”

Serotonin and the search for the anatomical substrate of aggression

“…The cell bodies of the identified 5HT-PLP neurons and their axons are located close to the posterior surface of the brain, while their projections are directed anteriorly to form three distinct arborization zones: one in the ventrolateral protocerebrum; a second in close proximity to the fan-shaped body of the central complex; and a third around the peduncles of the mushroom body near the ellipsoid body of the central complex ( Figure 1A). The densest arborization is in the ventrolateral protocerebrum, a region previously characterized as an integrative center for auditory, 15 visual, 16 and olfactory information processing. 17 More recently, this region also has been found to be important for courtship.…”