Microengineered devices enable long-term imaging of the ventral nerve cord in behaving adult Drosophila

Hermans, Laura; Kaynak, Murat; Braun, Jonas; Ríos, Victor Lobato; Chen, Chin‐Lin; Friedberg, Adam; Günel, Semih; Aymanns, Florian; Sakar, Mahmut Selman; Ramdya, Pavan

doi:10.1038/s41467-022-32571-y

Cited by 14 publications

(14 citation statements)

References 73 publications

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“…10 ). In the future, it would be of great importance to obtain an even larger sampling of ANs in multiple behavioral contexts and to test the degree to which AN encoding is genetically hardwired or capable of adapting during motor learning or after injury 59 , 60 . Our finding that ANs encode behavioral states and convey these signals to integrative sensory and action selection centers in the brain may guide the study of ANs in the mammalian spinal cord 17 , 18 , 49 and also accelerate the development of more effective bioinspired algorithms for robotic sensory contextualization and action selection 2 .…”

Section: Discussionmentioning

confidence: 99%

Ascending neurons convey behavioral state to integrative sensory and action selection brain regions

et al. 2023

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Knowing one’s own behavioral state has long been theorized as critical for contextualizing dynamic sensory cues and identifying appropriate future behaviors. Ascending neurons (ANs) in the motor system that project to the brain are well positioned to provide such behavioral state signals. However, what ANs encode and where they convey these signals remains largely unknown. Here, through large-scale functional imaging in behaving animals and morphological quantification, we report the behavioral encoding and brain targeting of hundreds of genetically identifiable ANs in the adult fly, Drosophila melanogaster. We reveal that ANs encode behavioral states, specifically conveying self-motion to the anterior ventrolateral protocerebrum, an integrative sensory hub, as well as discrete actions to the gnathal ganglia, a locus for action selection. Additionally, AN projection patterns within the motor system are predictive of their encoding. Thus, ascending populations are well poised to inform distinct brain hubs of self-motion and ongoing behaviors and may provide an important substrate for computations that are required for adaptive behavior.

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Section: Discussionmentioning

confidence: 99%

Ascending neurons convey behavioral state to integrative sensory and action selection brain regions

et al. 2023

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“…For recording calcium signals in the VNC of behaving flies, we adapted a previously described preparation (Chen et al 2018; Hermans et al 2022). First, we clipped the fly’s wings under cold anesthesia.…”

Section: Methodsmentioning

confidence: 99%

Presynaptic inhibition selectively suppresses leg proprioception in behavingDrosophila

Dallmann,

Luo,

Agrawal

et al. 2023

Preprint

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The sense of proprioception is mediated by internal mechanosensory neurons that detect joint position and movement. To support a diverse range of functions, from stabilizing posture to coordinating movements, proprioceptive feedback to limb motor control circuits must be tuned in a context-dependent manner. How proprioceptive feedback signals are tuned to match behavioral demands remains poorly understood. Using calcium imaging in behavingDrosophila, we find that the axons of position-encoding leg proprioceptors are active across behaviors, whereas the axons of movement-encoding leg proprioceptors are suppressed during walking and grooming. Using connectomics, we identify a specific class of interneurons that provide GABAergic presynaptic inhibition to the axons of movement-encoding proprioceptors. These interneurons are active during self-generated but not passive leg movements and receive input from descending neurons, suggesting they are driven by predictions of leg movement originating in the brain. Predictively suppressing expected proprioceptive feedback provides a mechanism to attenuate reflexes that would otherwise interfere with voluntary movement.

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“…Code for two-photon data pre-processing can be found in the ‘twoppp’ Python package on GitHub previously used in ref. 82 . Code for more detailed analysis can be found in the GitHub repository for this paper.…”

Section: Methodsmentioning

confidence: 99%

“…Recordings from the thoracic cervical connective suffer from large inter-frame motion including large translations, as well as smaller, non-affine deformations. Contrary to motion correction procedures used before for similar data 82 , here we made use of the high baseline fluorescence seen in Dfd > LexAop-GCaMP6s animals instead of relying on an additional, red color channel for motion correction. Thus, we performed motion correction directly on the green GCaMP channel.…”

Section: Methodsmentioning

confidence: 99%

Networks of descending neurons transform command-like signals into population-based behavioral control

Braun,

Hurtak,

Wang-Chen

et al. 2023

Preprint

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To transform intentions into actions, movement instructions must pass from the brain to downstream motor circuits through descending neurons (DNs). These include small sets of command-like neurons that are sufficient to drive behaviors—the circuit mechanisms for which remain unclear. Here, we show that command-like DNs inDrosophiladirectly recruit networks of additional DNs to orchestrate flexible behaviors. Specifically, we found that optogenetic activation of command-like DNs previously thought to drive behaviors alone in fact co-activate larger populations of DNs. Connectome analysis revealed that this functional recruitment can be explained by direct excitatory connections between command-like DNs and networks of interconnected DNs in the brain. The size of downstream DN networks is predictive of whether descending population recruitment is necessary to generate a complete behavior: DNs with many downstream descending partners require network recruitment to drive flexible behaviors, while neurons with fewer partners can alone drive stereotyped behaviors and simple movements. Finally, DN networks reside within behavior-specific clusters that inhibit one another. These results support a mechanism for command-like descending control whereby a continuum of stereotyped to flexible behaviors are generated through the recruitment of increasingly large DN networks which likely construct a complete behavior by combining multiple motor subroutines.

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Microengineered devices enable long-term imaging of the ventral nerve cord in behaving adult Drosophila

Cited by 14 publications

References 73 publications

Ascending neurons convey behavioral state to integrative sensory and action selection brain regions

Ascending neurons convey behavioral state to integrative sensory and action selection brain regions

Presynaptic inhibition selectively suppresses leg proprioception in behavingDrosophila

Networks of descending neurons transform command-like signals into population-based behavioral control

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