Navigating the waters – A neural systems approach to spatial cognition in fish

In 2014, the Nobel Prize in Physiology was awarded for the discovery of place and grid cells that process spatial cues in the mammalian hippocampal formation;, the key structure for both navigation and episodic memory1. Place and grid cells, and additional cell types form the central building blocks in the current circuit models of navigation in mammals. However, a cohesive picture of how these circuits compute space and enable navigation has not been achieved. In fact, emerging evidence suggest that these navigation circuits are highly diverse in cellular phenotypes and functionality; they do not only map aspects of space but also elements like sound, time, and reward. How neural systems of spatial cognition have evolved outside of the mammalian clade is not clear, and comparative studies are critically needed to gain insights to basic functional constraints and structural requirements underlying these neural circuits. The international research team of four PIs proposes a broad comparative systems neurobiological approach using teleost fish for integrative studies on higher navigation circuits. These fish are ideal models because they have conquered diverse spatial ecologies and show highly specialized sensory adaptions. Also, their brains exhibit an overall lower complexity to mammals, and are highly accessible to experimental manipulation. To establish systematic research on teleostean spatial cognition, the project combines neuroethological, electrophysiological, neuroimaging, and computational methodologies. Introducing a powerful electrophysiological recording technology in freely-moving fish and generating long-needed anatomical atlas resources, the project analyzes four teleost species with differing spatial ecologies. The team will uncover how different sensory modalities like vision, perception of depth, and active electrolocation are integrated during spatial navigation tasks, thereby investigating how top-down mechanisms modulate sensory integration of spatial learning. Finally, the team will test specific hypotheses developed in small-scaled laboratory setups in an unconstrained natural environment. Here, the group will measure the activity of neurons in freely moving fish that explore a coral reef habitat. This will be the first ever attempt to analyze brain activity underlying navigation in the wild. Altogether, the project will provide new perspectives on the evolution, function, and mechanism of memory systems in animal navigation.