Oxytocin-mediated social preference and socially reinforced reward learning in the miniature fishDanionella cerebrum

Abstract

The rapid adoption of the larval zebrafish as a systems neuroscience model has been driven largely by its small size and optical transparency, which enable the use of imaging and optogenetics techniques to record and manipulate activity throughout the brain.Unfortunately, larval fish lack the mature behavioral repertoire of adults and so a number of learning phenomena and social behaviors cannot be investigated in these animals.Here we establish the pedomorphic fish species Danionella translucida as a laboratory model that overcomes this limitation. Adult Danionella possess the size and optical transparency of late-larval zebrafish, which we exploit to image deep within the brains of a behaviorally mature animals using two-photon microscopy. The close phylogenetic relationship between Danionella and zebrafish enabled us to use existing reagents and techniques for transgenesis, and zebrafish-derived enhancer elements drove transgene expression in Danionella with their intended specificities. In a behavioral assay for socially-reinforced place preference, interactions between fish were found to be positively reinforcing and dependent on gender, demonstrating the power of this species for studies of learning and memory as well as social behavior. The establishment of Danionella's behavioral, molecular, and optical tractability provides a unique opportunity for researchers seeking to understand the relationship between circuits and adult-onset behaviors at a whole-brain level.

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

“…Members of this miniaturized group are developmentally arrested and resemble larval Danios in several ways: adult Danionellas lack scales, barbels and many typically late-ossifying bones (Britz, Conway et al 2009, Britz andConway 2016), and they retain a larva-like pigment pattern and feeding kinematics (McMenamin, Carter et al 2017, Galindo, Sweet et al 2018. Danionellas are emerging as a novel model for studying behavior, neurobiology and brain function (Penalva, Bedke et al 2018, Schulze, Henninger et al 2018, and a hybrid genome assembly was recently completed (Kadobianskyi, Schulze et al 2019). A better understanding of the relationships between Danionellas and developing zebrafish, along with insights into the pathways that may underlie the group's remarkable developmental arrest, will inform a better grasp of this emerging model.…”

Evolutionary divergence of locomotion in two related vertebrate species

“…Danionella translucida (DT) are minute cyprinid fish that show an extreme case of organism-wide progenesis or developmental truncation which leads to a small adult body size combined with a partially developed cranium without a skull roof. This feature together with its transparency throughout the adult stages makes them interesting for functional neuroscience studies allowing the imaging of the entire brain at cellular resolution 3,4 . However, studies on ossification in Danionella sp.…”

“…transparency throughout the adult stages makes them interesting for functional neuroscience studies allowing the imaging of the entire brain at cellular resolution 3,4 . However, studies on ossification in Danionella sp.…”

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in danionins

“…Danionella is miniaturized and developmentally arrested, resembling larval zebrafish in several ways: adult Danionella lack scales, barbels, and many typically late‐ossifying bones, and retain a larva‐like pigment pattern and feeding kinematics . Danionella translucida is emerging as a novel model for studying behavior, neurobiology, and brain function, and a hybrid genome assembly was recently completed . A better understanding of the developmental relationships between Danionella and zebrafish, along with information about the pathways underlying paedomorphosis in Danionella , will offer new insights about this emerging model.…”