Dimensionality reduction reveals separate translation and rotation populations in the zebrafish hindbrain

Curr Biol. 2023 Sep 25;33(18):3911-3925.e6. doi: 10.1016/j.cub.2023.08.037. Epub 2023 Sep 8.

Abstract

In many brain areas, neuronal activity is associated with a variety of behavioral and environmental variables. In particular, neuronal responses in the zebrafish hindbrain relate to oculomotor and swimming variables as well as sensory information. However, the precise functional organization of the neurons has been difficult to unravel because neuronal responses are heterogeneous. Here, we used dimensionality reduction methods on neuronal population data to reveal the role of the hindbrain in visually driven oculomotor behavior and swimming. We imaged neuronal activity in zebrafish expressing GCaMP6s in the nucleus of almost all neurons while monitoring the behavioral response to gratings that rotated with different speeds. We then used reduced-rank regression, a method that condenses the sensory and motor variables into a smaller number of "features," to predict the fluorescence traces of all ROIs (regions of interest). Despite the potential complexity of the visuo-motor transformation, our analysis revealed that a large fraction of the population activity can be explained by only two features. Based on the contribution of these features to each ROI's activity, ROIs formed three clusters. One cluster was related to vergent movements and swimming, whereas the other two clusters related to leftward and rightward rotation. Voxels corresponding to these clusters were segregated anatomically, with leftward and rightward rotation clusters located selectively to the left and right hemispheres, respectively. Just as described in many cortical areas, our analysis revealed that single-neuron complexity co-exists with a simpler population-level description, thereby providing insights into the organization of visuo-motor transformations in the hindbrain.

Keywords: behavior; conjugate; dimensionality reduction; hindbrain; imaging; oculomotor; optokinetic; regression; sensorimotor; vergence; zebrafish.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / physiology
  • Rhombencephalon* / physiology
  • Rotation
  • Swimming
  • Zebrafish* / physiology