Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion

Abstract

In the absence of salient sensory cues to guide behavior, animals must still execute sequences of motor actions in order to forage and explore. How such successive motor actions are coordinated to form global locomotion trajectories is unknown. We mapped the structure of larval zebrafish swim trajectories in homogeneous environments and found that trajectories were characterized by alternating sequences of repeated turns to the left and to the right. Using whole-brain light-sheet imaging, we identified activity relating to the behavior in specific neural populations that we termed the anterior rhombencephalic turning region (ARTR). ARTR perturbations biased swim direction and reduced the dependence of turn direction on turn history, indicating that the ARTR is part of a network generating the temporal correlations in turn direction. We also find suggestive evidence for ARTR mutual inhibition and ARTR projections to premotor neurons. Finally, simulations suggest the observed turn sequences may underlie efficient exploration of local environments.

DOI: http://dx.doi.org/10.7554/eLife.12741.001

eLife digest

Much of an animal’s behavior is guided by cues in the environment: many animals follow odors to find food, for example. But even in the absence of such cues, animals continue to show spontaneous behaviors that are optimized to help them discover resources, such as food, or landmarks, such as shelter. While these behaviors have been observed in many animals, it is unclear how they are supported by the nervous system. This is partly because it is hard to know where to look for relevant signals in large brains of many animals.

The development of whole-brain imaging techniques in zebrafish larvae offers a possible solution to this problem. Zebrafish are commonly used in laboratory studies because the zebrafish genome has been fully sequenced and they reproduce quickly. Whole-brain imaging in larval zebrafish has previously revealed widespread and complex patterns of spontaneous activity. However, it has been unclear whether or how these ‘thoughts’ are translated into behavior. Moreover, while researchers have studied how the fish respond to lights and sounds, little is known about how fish behave in the absence of guiding stimuli from their environment.

Dunn, Mu et al. now show that spontaneous fish behavior is not random, but is instead characterized by alternating states in which the fish are more likely to repeatedly turn either left or right. Simulations show that this pattern of swimming increases the fish's local foraging efficiency. By analyzing data from across the whole brain, Dunn, Mu et al. identified specific circuits of neurons that help generate these switching chains of turns. This alternating left-right rhythm appears to be dictated by signals sent between theses sets of neurons and may be supported by feedback from the behavior itself.

This analysis generates specific predictions about how specific neurons should connect with one another, and about the relationship between this connectivity and the activity of the rest of the brain. Future studies are required to test these predictions, and to determine how factors – such as whether an animal is hungry, for example – influence the pattern of spontaneous movements.

DOI: http://dx.doi.org/10.7554/eLife.12741.002