Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Abstract

Diverse subpopulations of mechanosensory neurons detect different mechanical forces and influence behavior. How these subpopulations connect with central circuits to influence behavior remains an important area of study. We previously discovered a neural circuit that elicits grooming of the Drosophila melanogaster antennae that is activated by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations and define how they interface with the circuit that elicits antennal grooming. We show that the subpopulations project to distinct zones in the brain and differ in their responses to mechanical stimulation of the antennae. Each subpopulation elicits grooming through direct synaptic connections with a single interneuron in the circuit, the dendrites of which span the different mechanosensory afferent projection zones. Thus, distinct JO subpopulations converge onto the same neural circuit to elicit a common behavioral response.The fruit fly (Drosophila melanogaster) Johnston's organ (JO) is a chordotonal organ in the antennae that can be studied to address this outstanding question. The JO detects diverse types of subpopulations are each known to consist of morphologically heterogeneous JON types that have not been completely described (Kamikouchi et al., 2006), we first define their morphological diversity by reconstructing major portions of each subpopulation from an EM volume of the fly brain (Zheng et al., 2018). We next produce transgenic driver lines that selectively target expression in each subpopulation. These lines enable us to visualize the distribution of the different subpopulations in the antennae and determine that they respond differently to mechanical stimuli. Optogenetic activation experiments confirm our previous finding that each JON subpopulation can elicit grooming of the antennae (Hampel et al., 2015). However, we report here that one of the subpopulations also elicits an avoidance response, whereas the other elicits wing flapping movements. Finally, by employing EM reconstructions and functional imaging experiments, we determine that JONs within each subpopulation are synaptically and functionally connected with the antennal command circuit through the same interneuron (aBN1). These results provide a comprehensive description of the topography of the JO, and reveal how different JON subpopulations whose projections occupy different points in topographical space can converge on the same neural circuit to elicit a similar behavioral response. Results and discussion Electron microscopy-based reconstruction of different JON subpopulationsWe first sought to define the morphological diversity of the neurons within each JON subpopulation as a prerequisite for understanding how the subpopulations interface with the antennal command circuit. JONs project from the antennae through the antennal nerve into a region of the SEZ called the antennal mechanosensory and motor ce...

Somatotopic organization among parallel sensory pathways that promote a grooming sequence in Drosophila

“…The aDNs project to a zone in the VNC where circuitry for generating antennal grooming leg movement patterns is thought to reside ( Berkowitz and Laurent, 1996 ). While this circuit is postsynaptic to the JONs ( Hampel et al, 2020b ; Hampel et al, 2015 ), preliminary connectomic analysis reveals that it is also postsynaptic to BMNs (not shown). Future studies will define the BMN connectivity with the antennal grooming circuit, and other neurons (and circuits) whose activation elicit aimed grooming of different head locations.…”

“…Second, previous studies showed that optogenetic activation of different sensory and interneuron types elicits grooming of specific head locations, suggesting that they are components of putative parallel circuits ( Cande et al, 2018 ; Guo et al, 2022 ; Hampel et al, 2015 ; Seeds et al, 2014 ; Zhang et al, 2020 ). Third, we identified different neuron types whose activation elicit grooming of the antennae and showed that they are connected to form a neural circuit ( Hampel et al, 2020b ; Hampel et al, 2015 ). The inputs to this circuit are JONs that detect tactile stimulations of the antennae and project to the SEZ where they excite two interneuron types (aBN1 and aBN2) and a descending neuron type (aDN) to elicit grooming.…”

Somatotopic organization among parallel sensory pathways that promote a grooming sequence inDrosophila

“…The aDNs project to a zone in the VNC where circuitry for generating antennal grooming leg movement patterns is thought to reside (Berkowitz and Laurent, 1996). While this circuit is postsynaptic to the JONs (Hampel et al, 2020b, 2015), preliminary connectomic analysis reveals that it is also postsynaptic to BMNs (not shown). Future studies will define the BMN connectivity with the antennal grooming circuit, and other neurons (and circuits) whose activation elicit aimed grooming of different head locations.…”

“…Second, previous studies showed that optogenetic activation of different sensory and interneuron types elicits grooming of specific head locations, suggesting that they are components of putative parallel circuits (Cande et al, 2018; Guo et al, 2022; Hampel et al, 2015; Seeds et al, 2014; Zhang et al, 2020). Third, we identified different neuron types whose activation elicit grooming of the antennae and showed that they are connected to form a neural circuit (Hampel et al, 2020b, 2015). The inputs to this circuit are JONs that detect tactile stimulations of the antennae and project to the SEZ where they excite two interneuron types (aBN1 and aBN2) and a descending neuron type (aDN) to elicit grooming.…”