Representation of Borders and Swimming Kinematics in the Brain of Freely-Navigating Fish
Like most animals, the survival of fish depends crucially on navigation in space. This capacity has been documented in numerous behavioral studies that have revealed navigation strategies and the sensory modalities used for navigation. However, virtually nothing is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a novel wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. Four cell types were identified: border cells, head direction cells, speed cells and conjunction head direction with speed. Border cells were active when the fish was near the boundary of the environment. Head direction cells were shown to encode head direction. Speed cells only encoded the absolute speed independent of direction suggestive of an odometry signal. Finally, the conjunction of head direction with speed cells represented the velocity of the fish. This study thus sheds light on how information related to navigation is represented in the brain of swimming fish, and addresses the fundamental question of the neural basis of navigation in this diverse group of vertebrates. The similarities between our observations in fish and earlier findings in mammals may indicate that the networks controlling navigation in vertebrate originate from an ancient circuit common across vertebrates. Summary Navigation is a fundamental behavioral capacity facilitating survival in many animal species. Fish is one lineage where navigation has been explored behaviorally, but it remains unclear how freely swimming fish represent space and locomotion in the brain. This is a key open question in our understanding of navigation in fish and more generally in understanding the evolutionary origin of the brain’s navigation system. To address this issue, we recorded neuronal signals from the brain of freely swimming goldfish and successfully identified representations of border and swimming kinematics in a brain region known to be associated with navigation. Our findings thus provide a glimpse into the building blocks of the neural representation underlying fish navigation. The similarity of the representation in fish with that of mammals may be key evidence supporting a preserved ancient mechanism across brain evolution.
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