Neural dynamics and architecture of the heading direction circuit in a vertebrate brain

Abstract

Animals can use different strategies to navigate. They may guide their movements by relying on external cues in their environment or, alternatively, by using an internal cognitive map of the space around them and their position within it. An essential part of this representation are heading cells, neurons whose activity depends on the heading direction of the animal. Although those cells have been found in vertebrates, the full network has never been observed and there is very little mechanistic understanding of how these cells acquire their response properties. In this study, we use volumetric functional imaging in larval zebrafish to observe, for the first time in a vertebrate, a full network that encodes allocentric heading direction. This network of approximately one hundred inhibitory neurons is arranged in an anatomical circle in the anterior hindbrain. Its activity is driven purely by the integration of internally generated signals, indicating that a simple vertebrate brain can encode maps of how an animal moves within its surroundings. Single cell reconstructions of electron micrographs allow us to uncover how the connectivity pattern of neurons within the network supports the implementation of a ring attractor network. The neurons we identify share features with neurons in the dorsal tegmentum nucleus of rodents and the fly central complex, showing that similar connectivity and mechanistic principles underlie the generation of cognitive maps of heading direction across the animal kingdom.

A cortico-collicular circuit for accurate orientation to shelter during escape

“…Similar models have been previously applied to explain tuning specificity in sensory pathways, including visual 30 , somatosensory 31 and auditory 32 ; as well as to the representation of saccadic vectors between the frontal eye field and the SC 33 . Our model is also closely related to models of heading direction in a variety of circuits and animals species 27,34 , perhaps suggesting a conserved circuit architecture for mapping circular variables.…”

Converting an allocentric goal into an egocentric steering signal

“…For example, neural correlates of moment-to-moment heading (i.e. head-direction cells) exist in vertebrates 1,19,20 and invertebrates 2,21,22 as do neurons with activity related to navigational goals 10,11,23,24 and locomotor turns 25–27 . Yet, despite these correlates and associated computational models for goal-directed navigation 18,27–30 a biological circuit that converts allocentric, navigation-related signals into an output appropriate for the motor system has yet to be described.…”

Neural representation of goal direction in the monarch butterfly brain

“…Consequently, their brain constantly compares the current heading direction with the goal direction (Dacke and el Jundi, 2018; Honkanen et al, 2019). While the former is encoded by evolutionarily conserved head-direction (HD) neurons found in different species (Beetz et al, 2022; Ben-Yishay et al, 2021; Geva-Sagiv et al, 2015; Hulse and Jayaraman, 2020; Petrucco et al, 2022; Seelig and Jayaraman, 2015; Takahashi et al, 2022; Taube et al, 1990; Varga and Ritzmann, 2016; Vinepinsky et al, 2020), goal-direction (GD) neurons whose action potential rate correlates with the animal’s goal direction have only been reported in the mammalian brain (Sarel et al, 2017). However, even in the tiny brain of an insect, a robust representation of the goal direction is of the highest ecological importance.…”