Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning in<i>Drosophila</i>

Ehweiner, Andreas; Brembs, Björn

doi:10.1101/2022.12.16.520755

“…The overlap (or lack thereof) may not be clearly visible in these 2D renderings presented in this text, which is why we made the 3D image stacks available for closer scrutiny (DOI: 10.5281/zenodo.10047941). 79 Both the C380-Gal4 driver used in Figure 1 and the D42-Gal4 driver used here, label not only MNs but also other neurons, in particular cholinergic neurons. However, the lines overlap in MNs in the VNC.…”

Section: Resultsmentioning

confidence: 99%

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila

Ehweiner,

Duch,

Brembs

2024

F1000Res

0

View full text Add to dashboard Cite

Background Motor learning is central to human existence, such as learning to speak or walk, sports moves, or rehabilitation after injury. Evidence suggests that all forms of motor learning share an evolutionarily conserved molecular plasticity pathway. Here, we present novel insights into the neural processes underlying operant self-learning, a form of motor learning in the fruit fly Drosophila. Methods We operantly trained wild type and transgenic Drosophila fruit flies, tethered at the torque meter, in a motor learning task that required them to initiate and maintain turning maneuvers around their vertical body axis (yaw torque). We combined this behavioral experiment with transgenic peptide expression, CRISPR/Cas9-mediated, spatio-temporally controlled gene knock-out and confocal microscopy. Results We find that expression of atypical protein kinase C (aPKC) in direct wing steering motoneurons co-expressing the transcription factor FoxP is necessary for this type of motor learning and that aPKC likely acts via non-canonical pathways. We also found that it takes more than a week for CRISPR/Cas9-mediated knockout of FoxP in adult animals to impair motor learning, suggesting that adult FoxP expression is required for operant self-learning. Conclusions Our experiments suggest that, for operant self-learning, a type of motor learning in Drosophila, co-expression of atypical protein kinase C (aPKC) and the transcription factor FoxP is necessary in direct wing steering motoneurons. Some of these neurons control the wing beat amplitude when generating optomotor responses, and we have discovered modulation of optomotor behavior after operant self-learning. We also discovered that aPKC likely acts via non-canonical pathways and that FoxP expression is also required in adult flies.

show abstract

“…Underlying data for 'Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila', University of Regensburg: 6B: https://www.doi.org/10.5283/epub.52964 94 University of Regensburg: 7A: https://www.doi.org/10.5283/epub.52947 107 University of Regensburg: 7B: https://www.doi.org/10.5283/epub.53685 108 Data are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).…”

Section: Data Availabilitymentioning

confidence: 99%

“…Both flies that were fed the steroid hormone RU486 (left, yellow) and the genetically identical flies without the hormone (right, green), showed high PIs, low p-values and high Bayes Factors, indicating a preference for the unpunished torque domain. Data: 10.5283/epub.52947 107. B.…”

mentioning

confidence: 99%

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila

Ehweiner,

Duch,

Brembs

2024

F1000Res

0

View full text Add to dashboard Cite

Background Motor learning is central to human existence, such as learning to speak or walk, sports moves, or rehabilitation after injury. Evidence suggests that all forms of motor learning share an evolutionarily conserved molecular plasticity pathway. Here, we present novel insights into the neural processes underlying operant self-learning, a form of motor learning in the fruit fly Drosophila. Methods We operantly trained wild type and transgenic Drosophila fruit flies, tethered at the torque meter, in a motor learning task that required them to initiate and maintain turning maneuvers around their vertical body axis (yaw torque). We combined this behavioral experiment with transgenic peptide expression, CRISPR/Cas9-mediated, spatio-temporally controlled gene knock-out and confocal microscopy. Results We find that expression of atypical protein kinase C (aPKC) in direct wing steering motoneurons co-expressing the transcription factor FoxP is necessary for this type of motor learning and that aPKC likely acts via non-canonical pathways. We also found that it takes more than a week for CRISPR/Cas9-mediated knockout of FoxP in adult animals to impair motor learning, suggesting that adult FoxP expression is required for operant self-learning. Conclusions Our experiments suggest that, for operant self-learning, a type of motor learning in Drosophila, co-expression of atypical protein kinase C (aPKC) and the transcription factor FoxP is necessary in direct wing steering motoneurons. Some of these neurons control the wing beat amplitude when generating optomotor responses, and we have discovered modulation of optomotor behavior after operant self-learning. We also discovered that aPKC likely acts via non-canonical pathways and that FoxP expression is also required in adult flies.

show abstract

Neuronal circuit mechanisms of competitive interaction between action-based and coincidence learning

Rozenfeld,

Parnas

2024

Sci. Adv.

0

View full text Add to dashboard Cite

How information is integrated across different forms of learning is crucial to understanding higher cognitive functions. Animals form classic or operant associations between cues and their outcomes. It is believed that a prerequisite for operant conditioning is the formation of a classical association. Thus, both memories coexist and are additive. However, the two memories can result in opposing behavioral responses, which can be disadvantageous. We show that Drosophila classical and operant olfactory conditioning rely on distinct neuronal pathways leading to different behavioral responses. Plasticity in both pathways cannot be formed simultaneously. If plasticity occurs at both pathways, interference between them occurs and learning is disrupted. Activity of the navigation center is required to prevent plasticity in the classical pathway and enable it in the operant pathway. These findings fundamentally challenge hierarchical views of operant and classical learning and show that active processes prevent coexistence of the two memories.

show abstract

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Cited by 3 publications

References 168 publications

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant self-learning in Drosophila

Neuronal circuit mechanisms of competitive interaction between action-based and coincidence learning

Contact Info

Product

Resources

About