Strategies used by two memories to share space in a common neural network

Abstract

How distinct memories are encoded into the same network space without destructive interference is not well-understood. Here, we utilized Tritonia diomedeas escape swim network to explore how two sequentially acquired forms of non-associative learning, sensitization and habituation, are encoded into the same network. Behavioral experiments showed them to alter non-identical sets of behavioral features, suggesting they utilize somewhat independent sites of plasticity within the network. Large-scale voltage-sensitive dye recordings revealed two findings. First, both forms of learning, which occur sequentially in the 10-trial training protocol used, act to produce a change in the number of pedal neurons firing during the dorsal phase of the motor program, with sensitization producing an increase, and habituation a decrease in their number. The number of neurons participating in the ventral phase was unaffected. Second, sensitization produced an enhancement of burst intensity specific to the ventral phase neurons, while habituation was associated with a decrease in burst intensity in both phases. Using injected current pulses, intracellular recordings revealed that sensitization acted to increase the excitability of neurons firing in both phases, whereas habituation only acted to reduce excitability in ventral phase neurons. These excitability changes were associated with different mechanisms - reduced spike frequency accommodation in the ventral phase neurons, and depolarization of the resting potential in the dorsal phase neurons. These findings of partially different storage sites and mechanisms for two different non-associative memories illuminate a potential network strategy for minimizing destructive interference when storing multiple memories into the same network.