Most animals, including humans, have the ability to know their current location relative to a starting point through a process called path integration. Essentially, they add up (or integrate) all of the movements they make on their outward journey, store this calculation in memory, and use it to return to their starting point. This project aims to dissect the currently unknown sensory and motor mechanisms of path integration and how this process works in relation to two other behaviors with which it is critically intertwined: 1) reflexes that maintain physical and perceptual stability (e.g., the vestibuloocular reflex), and 2) spatially dependent social behavior. Fiddler crabs are an ideal system for studying the mechanisms underlying path integration, since through path integration they form the strictest spatial relationship with home of any animal. Until recently fiddler crabs were thought only to form a strong attachment to their own burrow, but new evidence shows some species remember the locations of several burrows simultaneously. This disparity in spatial memory corresponds with the two major mating systems in the genus, and recent experiments suggest that species from each system have fundamentally different path integration mechanisms that incorporate eye- and body-stabilizing reflexes differently. Spatial orientation mechanisms appear to have co-evolved with changes in mating systems to produce spatial navigation abilities that uniquely adapt a species for its social and ecological contexts. This research will provide a uniquely integrative understanding of the interdependent evolution of spatial cognition and social behavior.

The results from this research will answer fundamental concepts in spatial cognition and spatial orientation that will broadly impact the engineering of task-oriented machines. Results on how spatial navigation has evolved to varying degrees of task-dependent complexity have the potential to be materially applied, particularly for the design of robots whose ability to reflexively compensate for disturbances is fully incorporated into their ability to perform path integration. The project will train graduate students, and undergraduate students from minorities underrepresented in the sciences through the Student Achievement in Research and Scholarship (STARS) and Women in Science and Engineering (WISE) programs.

Project Report

When an animal leaves its home, how does it find its way back again? There are several different ways of accomplishing this, each of which is like an algorithm in the animal’s brain. The algorithm takes in sensory information about movement, and computes the current coordinates relative to home or, equivalently, the coordinates of home relative to the animal. Different animals have different algorithms. They differ in the input they use (e.g., vision, acceleration, leg movements, etc.), and how they use it – some use more than one input simultaneously, others only one, some appear to compute a mathematically precise location while others seem to compute it in an imprecise way. All of these ‘choices’ about how to compute the location of home make a difference; some are simple and so probably quick and cheap, but may be unable to overcome disturbances or errors, others are more complicated but more versatile and robust. We sought to discover whether different algorithms conferred different navigation abilities on their owners that were ecologically and evolutionarily important. Fiddler crabs are ideal for this study, because early observations hinted that closely related species apparently have different algorithms. Also, the two species differed in another important way: in one species the males and females courted one another in a way that required only the simplest sort of navigational ability, but the other species had a more sophisticated sense of the space around them and their homes (burrows in the sand). We wondered whether the two species had different courtship behavior because, basically, their spatial algorithms allowed or disallowed certain behaviors. First we wanted to find out how fiddler crabs measure movements, i.e., what is the input into the algorithm? There are two things the crabs must measure about locomotion: distance, and direction. Start with distance. To measure distance, they could use one or more sensory cues – vision (viewing the moving ground under foot), vestibular sensation (acceleration and deceleration), proprioception (sensors in the limbs that reflect the position and movement of the limbs). There is even a fourth, non-sensory option – they could remember what they tried to do, rather than measuring what they actually did. These two things are normally the same, but not always. By making the crabs run home over a ‘crab treadmill’ we demonstrated that the sensory signals used by the algorithm are not visual or vestibular. They come from either leg proprioceptors, or commands to the locomotory sytem from the CNS. As part of the study of distance measurement, we asked whether the crabs could measure distances over bumpy terrain, even when they had not encountered this before. We waited for them to leave their burrows on foraging expeditions, and forced them to run home over the top of a large hill. This forced them to take more steps to reach the right distance; did they know this and take it into account, or was their algorithm too simple to deal with novel terrain? We found that they knew with great accuracy how the hill affected their path, and made exactly the right adjustment in step number to get the right distance. This has important implications – it means that they measured not only their movements as they ran, but their body orientation at the moment each movement occurred. So, gravity must also be an important sensory input to the algorithm in their brains. How do fiddler crabs measure the direction in which they move? To answer this question we needed to either rotate the crab relative to the directional cues it normally uses, or rotate the directional cues relative to the crab. Not knowing exactly which directional cues the animal uses in the natural environment, we opted to rotate the crab relative to all of them at once – on a rotating disk in the sand. Interestingly, the crabs had a reflexive response to this, in which they actively counter-rotated, in order to remain in their original orientation. If they were successful, they went straight home. This is a very important finding, because it means that all the locomotion they performed in order to stay put was not sent into the algorithm – the animal only sends sensory information to the algorithm that is derived from voluntary movements, and not involuntary ones, even if the latter are massive! If we overcame the vigorous counter-rotation reflexes and got the animals out of orientation, they missed their burrow by an angle equal to the amount that we rotated them. This is also in important finding, because it means the animals don’t use external directional cues, but only measure the direction of their steps relative to their own bodies! So, they could measure direction using the same senses (or CNS commands) as measuring distance (we are working on this out right now).

Agency
National Science Foundation (NSF)
Institute
Division of Integrative Organismal Systems (IOS)
Application #
0749768
Program Officer
David Coppola
Project Start
Project End
Budget Start
2008-03-01
Budget End
2013-02-28
Support Year
Fiscal Year
2007
Total Cost
$379,998
Indirect Cost
Name
University of Cincinnati
Department
Type
DUNS #
City
Cincinnati
State
OH
Country
United States
Zip Code
45221