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Developmental biology - The Brain

How Brain Neurons Guide Muscle Movement

A single neuron triggers new behavior, while suppressing an opposite behavior...


Mapping nerve circuitry that smoothly and rapidly switches forward to backward movement is unprecedented according to Chris Doe, biology professor and co-director of the University of Oregon's Institute of Neuroscience. Doe investigated brain neurons in the fruit fly, observing how a single pair of neurons commands locomotion in both larvae and adults. His group's findings are published in the journal eLife.
"The big step we observed is how a single neuron both triggers a new behavior and suppresses an antagonistic behavior. Our finding that the same pair of neurons control crawling of a limbless maggot and walking of an adult fly was quite surprising."

Chris Q Doe PhD, Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon (UO), Eugene, Oregon, USA; member of UO's Institute of Molecular Biology.
Doe's lab was already looking at neurons tied to navigation behavior in fruit flies. Just how neural circuits trigger smooth switching between antagonistic behaviors is a mystery in most animals according to Doe, though it had been seen in nematodes (small worms). His seven-member research team used genetic screening, electron microscopy, optogenetics and manual manipulations on the project. They initially looked at 10 behavioral responses, but then focused on forward-backward motion. Fluorescent proteins inserted into larvae and adult flies helped them track chemical flows through neural circuitry as behaviors changed.

They methodically identified the two backward-inducing brain neurons, after observing more than 300 other neurons. Their biggest surprise, Doe adds, was realizing the same pair of neurons in a larva retracted connection to a suite of muscles during metamorphosis, but then re-engaged those motor neurons to the six legs that control muscles in its adult form. In limbless larvae, crawling is done by peristalsis, or rhythmic muscle contractions.
"Limbed locomotion involves a pattern of motion in legs that is completely different. All motor neurons are different in the two stages. Those in larvae are lost in metamorphosis. The brain neuron apparently recognizes this in both systems."

Chris Q Doe PhD.

That neuron, Doe observed, made halted forward motion but intense backward motion - and continuously. For escape purposes, one behavior must be rapidly inactivated by neural communication. Flies and mosquitoes, for instance, can sense a human's swat and change directions to avoid contact. Larvae can also recognize and avoid noxious environments - like high salt or bright light - using backwards locomotion.

"Until now, no one has shown that there is an upstream neuron that can coordinate the suppression of some behaviors while inducing others," he explains. "Our study gives other researchers a good example of what they may expect to find. A fly has many behaviors. The idea is to map the neurons and circuits controlling all."

Abstract
Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define 'command-like neuron' as a neuron whose activation elicits or 'commands' a specific behavior). In most animals it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval 'mooncrawler descending neurons' (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.

Authors: Arnaldo Carreira-Rosario, Aref Arzan Zarin, Matthew Q Clark, Laurina Manning, Richard D Fetter, Albert Cardona, and Chris Q Doe.

The authors declare no competing financial interests.


Funding
National Institutes of Health (HD27056)

Howard Hughes Medical Institute (HHMI)

A Porter Physiology Development Fellowship awarded to Clark in 2015-15 from the American Physiological Society also supported the work.

Note: The UO is equipped with an on-campus television studio with a point-of-origin Vyvx connection, which provides broadcast-quality video to networks worldwide via fiber optic network. There also is video access to satellite uplink and audio access to an ISDN codec for broadcast-quality radio interviews.

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Aug 30, 2018   Fetal Timeline   Maternal Timeline   News   News Archive




Cross section of a fruit fly ventral nerve (spinal) cord showing motor neurons involved in sensorimotor processing - those nerves that respond to a wasp and rapidly switch directions. Image: Chris Doe.


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