Already in the 1940s, behavioural scientists observed that animals divide complex behaviours, such as mating, into sub-tasks: to reproduce, a stickleback fish needs to decide whether to fight a rival, care for offspring or build on the nest. For nest building, it needs to dig a hole with its fins, which is further composed of many granular movements. However, in order to reach its long-lasting goal all these steps must be orchestrated. How a brain coordinates such hierarchical behaviours, and whether neurons also mirror this hierarchy, was unknown.
Neuroscientists from the lab of Manuel Zimmer, professor at the University of Vienna and group leader at the Research Institute of Molecular Pathology (IMP), now reported that hierarchical behaviour is controlled by hierarchical neuronal activity in the journal Neuron.
“Somehow, the brain must coordinate sub-tasks into a meaningful behaviour”, says Zimmer. “Until now, we didn’t know whether the neurons that regulate such hierarchies also act hierarchically - or rather sequentially.”
In their study, Manuel Zimmer and members of his research group, including Vienna BioCenter PhD students Harris Kaplan and Oriana Salazar Thula, used the nematode worm Caenorhabditis elegans as their model.
The worm’s nervous system comprises only 302 neurons and for each, the activity can be recorded in real-time. Moreover, C. elegans shows hierarchical behaviours: to crawl, the worm undulates its body, like a snake, in bends that take less than a second. With these undulations put together correctly, the worm either crawls forwards, backwards or turns, which is again assembled into longer behaviours like exploring.
Neuronal hierarchy controls crawling behaviour
In the present study, the authors used several existing microscopy techniques, which allowed them to observe the worm’s entire nervous system while determining which neuron is active at any given time. Doing so, they identified neural activity that correspond to each step in the behavioural hierarchy.
The neuroscientists found that three timescales of crawling behaviour are encoded in distinct neuronal activity patterns. At the highest level, neurons in the brain and the body decide between forward and backward crawling. On the next level, one set of motor neurons controls undulations, while on the lowest level another set of motor neurons controls head-casts, a quick flick of the worm’s head. These activities are nested, which means that the activity of neurons at the lower levels are controlled by the activity of neurons at the next highest level.
“This is not just about how a worm crawls in the soil”, Zimmer emphasizes, “but about the principles of how behaviours are organized by the brain. We have uncovered a hierarchy in an animal’s neuronal activity pattern.” These principles may be applicable beyond worms and other animals, Zimmer adds. “Human language is also organized hierarchically, with syllables, words and sentences. Potentially, the same principles might govern speech-generation and comprehension in the human brain.”
First author Harris Kaplan has already received two awards for his contribution to the study, the PhD Award of the Austrian Association of Molecular Life Sciences and Biotechnology and a Vienna BioCenter PhD Award.
Harris S. Kaplan, Oriana Salazar Thula, Niklas Khoss & Manuel Zimmer (2019). “Nested neuronal dynamics orchestrate a behavioral hierarchy across timescales.” Neuron, 28 November 2019. DOI: 10.1016/j.neuron.2019.10.037
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