MEMORY USE IN INSECT VISUAL NAVIGATION

Nature Reviews Neuroscience 3, 542 -552 (2002)
July 2002 Vol 3 No 7

Thomas S. Collett & Matthew Collett

Preface

The navigational strategies that are used by foraging ants and bees to reach a goal are similar to those of birds and mammals. Species from all these groups use path integration and memories of visual landmarks to navigate through familiar terrain. Insects have far fewer neural resources than vertebrates, so data from insects might be useful in revealing the essential components of efficient navigation. Recent work on ants and bees has uncovered a major role for associative links between long-term memories. We emphasize the roles of these associations in the reliable recognition of visual landmarks and the reliable performance of learnt routes. It is unknown whether such associations also provide insects with a map-like representation of familiar terrain. We suggest, however, that landmarks act primarily as signposts that tell insects what particular action they need to perform, rather than telling them where they are.

Summary

Insects use a mixture of strategies for their navigation. Some strategies involve little memory, and can be used for navigation through an unfamiliar environment. However, these early strategies may be inaccurate or slow. Later, more memory-intensive strategies can be faster or more accurate, but are possible only after multi-trial learning. Efficient multi-trial learning requires consistency of behaviour and sensory input. Early strategies aid learning by providing consistent routes and views. Once a territory becomes familiar and appropriate memories are available, later strategies that rely on these memories tend to take precedence over earlier strategies.
The two main families of strategies that are involved in visual navigation are view-based strategies and path integration. View-based strategies exploit prominent objects as landmarks to guide movement. An early view-based strategy is the use of landmarks as beacons. A later strategy is to use stored retinotopic snapshots of landmarks for image matching. Insects, such as ants and bees, can perform path integration using an odometer and a celestial compass to monitor the direction and distance travelled from a starting point. The early path-integration strategy is to measure the global vector between the nest and a food site. A later strategy is to use a sequence of learnt local vectors that correspond to path segments of a familiar route.
As an insect becomes familiar with a route, it often seems to divide the route into segments that are demarcated by landmarks. Navigation within the segment can be accurately controlled by a strategy that makes use of, for example, a single local vector, snapshot or beacon. Navigation along the total route will be accurate as long as the sequence can be followed reliably. For this, insects must recognize segments and recall appropriate actions reliably.
The recognition of path segments, like their learning, is aided by following consistent routes. The consistent viewing orientations simplify the recognition of landmarks. The recognition of a path segment is also aided by contextual cues, such as its consistent position in the sequence along the route, and the surrounding panoramic context.
The organization of memories that has been revealed so far seems to be well suited to navigating along familiar routes. Associations between memories seem to link memories along a route, and contextual cues can keep the memories of different routes separate. As yet, there is little evidence that memories are linked into a global map-like network.

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Author biographies

Thomas Collett is in the School of Biological Sciences at the University of Sussex. He has worked on problems that relate to the spatial vision of insects and, occasionally, other animals, using predominantly behavioural techniques.

Matthew Collett is a postdoctoral researcher at Michigan State University, where he studies navigation in honeybees. He obtained his doctorate at the University of Oxford in theoretical ecology, looking at how animal populations can be affected by interactions between individual behaviour and habitat spatial structure. Since then, he has been studying the cognitive underpinnings of spatial behaviour, concentrating on the use of path-integration memories in insect navigation