The sensory and cognitive basis of distance estimation in teleost fish

The ability to measure travel distances is central to navigating by path integration. A path integrating animal constantly and automatically sums movement vectors containing distance and direction self-motion information, providing it with a global vector home to a starting position. This allows the animal to at any time compute novel shortcuts through its familiar area, and reduces the reliance on external positional information to navigate.
Distance estimation has been widely documented in terrestrial animals at the sensory and neural mechanistic levels. In contrast, nothing is known about how freely-swimming aquatic animals such as the large vertebrate group - the teleost fish - collect and compute information on distance travelled. Understanding odometry in teleost fish is important first, for understanding the evolution of vertebrate spatial cognition from an aquatic common ancestor, and second, for understanding how aquatic animals more generally collect metric spatial information under the constraints and challenges of navigating underwater.
In this thesis, I study distance estimation in teleost fish for the first time. Using the Picasso triggerfish, Rhinecanthus aculeatus, I aim to answer two key questions: (i) Can teleost fish estimate distance travelled, and with what accuracy? (ii) What sensory mechanisms do teleost fish use to estimate distance travelled?
Using an operant conditioning task, I show that teleost fish can learn and remember travel distances with remarkable accuracy. This internal representation of distance travelled is also preferentially used over previously learned landmark cues when the two sources of information are in conflict.
I proceed to explore the sensory mechanisms underlying distance estimation in Rhinecanthus aculeatus. I show that Rhinecanthus is unlikely to use mechanosensory inputs from finbeats or measures of travel time for odometry. However, like many terrestrial animals, Rhinecanthus aculeatus relies strongly on self-induced optic flow to reproduce travel distances. Visual motion information is also used more broadly to control swimming speeds and to maintain straight, stable swimming trajectories. Therefore, despite the physical constraints water places on the scope of such sensory information, visual motion information can be as important for navigating underwater as it is on land. Unlike many terrestrial animals, teleost fish also have access to a second frame of reference from which they can measure travel distances: the water through which they swim. I finish by presenting preliminary evidence suggesting that in the absence of visual information Rhinecanthus can use sensory information from the water column itself to measure relative distance travelled.
This work provides an important baseline for understanding the mechanisms underlying distance estimation in teleost fish. Using the operant conditioning task developed in this thesis, we can study the neural basis of the teleost odometer and continue to test hypotheses about how metric spatial information is collected and encoded by teleost fish that are free to move without constraint through a volume.

Keywords: Teleost fish
Odometry
Optic flow
Path integration
Advisor: Burt de Perera, T