Azimuthal invariance to looming stimuli in the Drosophila giant fiber escape circuit

Abstract

Spatially invariant feature detection is a property of many visual systems that rely on visual information provided by two eyes. However, how information across both eyes is integrated for invariant feature detection is not fully understood. Here we investigate spatial invariance of looming responses in descending neurons (DNs) of Drosophila melanogaster. We find multiple looming responsive DNs integrate looming information across both eyes, even though their dendrites are restricted to a single visual hemisphere. One DN, the giant fiber (GF), responds invariantly to looming stimuli across tested azimuthal locations. We confirm visual information propagates to the GF from the contralateral eye through an unidentified pathway and demonstrate that the absence of this pathway alters GF responses to looming stimuli presented to the ipsilateral eye. Our data highlight a role for bilateral visual integration in generating consistent, looming-evoked escape responses that are robust across different stimulus locations and parameters.

Morphology and synapse topography optimize linear encoding of synapse numbers inDrosophilalooming responsive descending neurons

“…The resulting model parameters [capacitance (C m ), leak conductance (g leak ), axial resistivity (R a ), and reversal potential (E rev )] were found to be within physiological ranges (Borst and Haag, 1996;Gouwens and Wilson, 2009) and corresponded to other published models of Drosophila neurons (Gouwens and Wilson, 2009;Günay et al, 2015;Hafez et al, 2023;Liu et al, 2022). All 5 investigated DNs possess the capacity for action potential generation (Dombrovski et al, 2023;Jang et al, 2023;Namiki et al, 2018;Peek, 2018;von Reyn et al, 2017von Reyn et al, , 2014. These DNs therefore are predicted to feature a spike initiation zone (SIZ) characterized by a high concentration of voltage-gated sodium channels, whose principal alpha subunit is encoded by the para gene (Loughney et al, 1989).…”

“…Looming responsive DNs in Drosophila integrate retinotopic visual information from multiple VPNs. To uncover general principles for how VPN information is organized on DN dendrites, we selected five representative DNs demonstrated or predicted to be looming responsive for our analyses: DNp01, DNp02, DNp03, DNp04, and DNp06 (Dombrovski et al, 2023; Jang et al, 2023; Namiki et al, 2018; Peek, 2018; von Reyn et al, 2017, 2017). A connectivity analysis of the FAFB EM connectome (Zheng et al, 2018), shows that this population of DNs integrates looming information from six main VPN populations ( Figure 1B ) that have dendrites either only in the lobula (LC4, LC6, and LC22) or both in the lobula and lobula plate (LPLC1, LPLC2, and LPLC4) of the ipsilateral optic lobe.…”

“…All 5 investigated DNs possess the capacity for action potential generation (Dombrovski et al, 2023; Jang et al, 2023; Namiki et al, 2018; Peek, 2018; von Reyn et al, 2017, 2014). These DNs therefore are predicted to feature a spike initiation zone (SIZ) characterized by a high concentration of voltage-gated sodium channels, whose principal alpha subunit is encoded by the para gene (Loughney et al, 1989).…”

“…In vivo whole-cell, current-clamp electrophysiology was conducted on tethered flies as previously described (Jang et al, 2023; von Reyn et al, 2017). Flies were anesthetized by lowering the temperature to 4°C and their head and thorax were fixed to polyether-ether-ketone (PEEK) plates with UV glue (Loctite 3972).…”

Axon arrival times and physical occupancy establish visual projection neuron integration on developing dendrites in theDrosophilaoptic glomeruli

“…For adult whole-cell electrophysiology, female flies were head fixed to recording plates via UV glue, antenna were UV-glued, and the front legs were removed at the level of the femur as described previously 6,63 . GFP positive GF soma were accessed for recordings by removing the cuticle and overlying trachea, and then removing the perineural sheath by local application of collagenase (0.5% in extracellular saline).…”