Abstract

SummaryAnimals must frequently perform a sequence of behaviors to achieve a specific goal. However, the neural mechanisms that promote the continuation and completion of such action sequences are not well understood. Here, we characterize the anatomy, physiology, and function of the nucleus isthmi (NI), a cholinergic nucleus thought to modulate tectal-dependent, goal-directed behaviors. We find that the larval zebrafish NI establishes reciprocal connectivity with the optic tectum and identify two distinct types of isthmic projection neuron that either connect ipsilaterally to retinorecipient laminae of the tectum and pretectum or bilaterally to both tectal hemispheres. Laser ablation of NI caused highly specific deficits in tectally mediated loom-avoidance and prey-catching behavior. In the context of hunting, NI ablation did not affect prey detection or hunting initiation but resulted in larvae failing to sustain prey-tracking sequences and aborting their hunting routines. Moreover, calcium imaging revealed elevated neural activity in NI following onset of hunting behavior. We propose a model in which NI provides state-dependent feedback facilitation to the optic tectum and pretectum to potentiate neural activity and increase the probability of consecutive prey-tracking maneuvers during hunting sequences.

Highlights

  • To accomplish a behavioral goal, it is often necessary for an animal to execute a sequence of component actions

  • By using a virtual hunting assay combined with calcium imaging, we found that nucleus isthmi (NI) activity was recruited at the onset of hunting behavior

  • Because expression of cholinergic markers is a defining feature of NI across vertebrates [14], we examined expression of genes encoding proteins required for synthesis and vesicular transport of acetylcholine, which defines cholinergic neurons [16]

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Summary

Introduction

To accomplish a behavioral goal, it is often necessary for an animal to execute a sequence of component actions. Studies in various species have examined the organization and sequencing of behavioral elements in specific contexts [1]. Progress has been made identifying neural circuits involved in inducing specific behaviors, modulating features of behavior, and controlling the timing and serial execution of motor sequences (e.g., [2, 3]). Little is known about neural mechanisms that explicitly maintain a behavioral state so as to facilitate the progression of action sequences to support task completion. For complex behaviors, such as those involving interactions between animals, the sequence of sensory inputs might be less reliable. The presence of multiple prey might present competing stimuli that challenge the predator to sustain attention at a specific target

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