Scientists Detect Neural Circuit That Allows Self-insertion in Zebrafish

A multi-site brain circuit allows larval zebrafish to keep track of where they are, where they’ve been, and how they will return to their original position after being displaced, the researchers report in the journal Dec. Cell. The results shed light on how larval zebrafish track their position and use this to navigate after being deflected by currents.

“We studied a behavior in which larval zebrafish must remember past displacements to accurately maintain their position in space because, for example, water flow can drag them into dangerous areas of their natural habitat,” says senior author Misha Ahrens of the Janelia Research Campus. Howard Hughes Medical Institute. “Still, it is unknown whether they clearly track their location over long timescales and use memorized location information to return to their previous location – we call this behavior positional homeostasis. Such abilities may be ethologically critical because larval zebrafish swim intermittently and move with currents.” . during rest.”

Many animals keep track of where they are in their environment. They use their location information for many important behaviors, such as efficiently returning to safe places after visiting unknown and potentially dangerous areas, re-visiting food-rich areas, and avoiding foraging in food-poor areas. While self-positioning is represented in hippocampal formation, it is unknown how such representations arise, whether they exist in older brain regions and in what ways they control movement.

“Such circuits have been difficult to detect because neuroscience typically relies on recordings from cells in preselected brain regions that cover a small fraction of all neurons in the brain,” says first author En Yang, of the Howard Hughes Medical Institute, Janelia Research Campus.

In the new study, researchers set out to identify the complete navigation circuits in larval zebrafish, from movement integrators to premotor centers, by comprehensively imaging and analyzing the entire brain at cellular resolution during a self-positioning behavior. Access to over 100,000 neurons per animal revealed brain regions previously unknown to be involved in self-positioning, leading to the discovery of a multi-regional hindbrain circuit that mediates conversion from velocity to behavior through displacement memory.

“Our results reveal a nervous system for self-positioning and associated behavior in the vertebrate hindbrain and provide a circuit-level, representational, and control-theoretic understanding of its function. The system operates in a closed loop with dynamic environments,” Ahrens said. “These results demonstrate the need to consider brains at a holistic level and to combine systems neuroscience concepts – such as self-positioning and motor control – that are often studied separately.”

Whole-brain functional imaging revealed not only the presence of positional homeostasis in the larval zebrafish, but also how the brain identifies and corrects changes in zebrafish position. The underlying circuitry calculates its own position in the dorsal brainstem by integrating visual information to create a memory of past displacements as the animal actively or passively changes position. This self-position representation is read by the lower olive as a long-term positional error signal, reflecting the difference between the original and current position of the fish. This signal is converted to the locomotor output, which corrects for accumulated displacements over many seconds.

The authors say that this multisite circuitry has potential anatomical and functional homologs in mammals and may interact with other known representations of self-positioning. Moreover, this work links self-positioning and olivocerebellar motor control and establishes the vertebrate hindbrain as a neural control center for purposeful wayfinding behavior.

“Our results on location memory and spatial homeostasis resonate with the idea that evolutionarily ancient brain regions centrally contribute to higher-order behavior,” says Ahrens. “The idea that cognitive processes are widely distributed throughout the nervous system is in part compatible with the evolutionary premise that complex behavior emerges by building new circuits on top of old brain structures that do the relevant computations. Brain-wide studies of neural activity could thus be critical for identifying distributed mechanisms of cognitive function. “

This work was supported by the Howard Hughes Medical Institute and the Simons Foundation.

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