Memory Enhances Search Strategies During Odor-Guided Foraging

Abstract

Odor-guided searches are notoriously difficult due to the sparse and intermittent nature of odor plumes. However, rodents can adaptively modify their search strategy using internal representations of their dynamic environment. This allows for selecting the optimal strategy for making use of complex sensory cues to increase the effectiveness of odor-guided searches. To investigate this we constructed a large (2.5m x 1m) fully-automated open field arena that allowed us to distribute food pellets at precise locations throughout the arena without being restrained to defined reward locations. Using this system we precisely monitored search behavior while controlling the amount of information each animal had about possible pellet locations. To simulate nocturnal conditions Long-Evans rats foraged for sucrose pellets under far red light, which they cannot see, forcing them to rely upon olfactory cues to navigate. Rats were divided into two groups and were either trained on predictable or unpredictable pellet locations. Within a few days of training, all rats were able to complete the task quicker by decreasing their distance traveled and/or by increasing their velocity. Animals trained on the predictable, fixed condition had an increased number of efficient, stereotyped trajectories that persisted in the absence of pellets. To analyze phases of search, we sectioned trajectories by distance traveled into sequential 300cm bins. Animals trained on fixed distributions had significantly more correlated trajectories during the first bin compared to animals trained on random distributions. However, animals trained on fixed distributions were significantly impaired in navigating efficiently towards pellets located in slightly unpredictable areas, whereas animals trained on random distributions were only impaired when navigating to the most unpredictable pellets. Efficient performance recovered for all animals when they were about 40cm away from target pellet locations, suggesting this is the distance at which odor cues offer a directional benefit. Animals were then trained to forage for banana-scented sucrose pellets. When navigating to unpredictable pellets from a medium distance (20-80cm), animals had a significantly narrower angle of approach for banana-scented pellets compared to regular sucrose pellets, consistent with more intense odor cues guiding animals from a greater distance. These results suggest that rats form distinct foraging strategies based on learned probabilities of resource locations. Further, they can adaptively switch strategies during a single foraging bout, changing from a memory-based strategy to a strategy that relies on olfactory cues when resources are in unpredictable locations.