Misha Ahrens, Janelia Farm

Neural mechanisms underlying spontaneous and learned behavior in larval zebrafish

An animal’s actions are dependent on its current environment as well as on its past experiences. We sought to identify neural mechanisms underlying two types of history dependence in behavior of larval zebrafish. First, we studied sequences of spontaneous motor actions, where the choice of whether to swim left or right is strongly influenced by past swim patterns. We performed whole-brain imaging to discover groups of neurons that are necessary and sufficient for a short-term memory of turning direction. An excitatory-inhibitory circuit, storing heading direction in sustained activity, enables history-dependent, non-random choices of swim direction to implement an efficient local foraging strategy. Second, we studied a short-term form of motor learning, in which the animals learn changes in the relationship between their locomotor commands and the resulting distance moved, then adjust command strength to achieve a desired travel distance. We used whole-brain neuronal imaging and circuit manipulations to discover that the serotonergic dorsal raphe nucleus stores a short-term memory of learned swim vigor, in persistent activity of serotonergic neurons. This learned representation of the “effectiveness of actions” arises from integration of the sensory feedback from individual swim bouts, and transmission to behavior was raphe- and serotonin-dependent. These studies reveal that experience-dependence in spontaneous behavior and motor learning in zebrafish is implemented through combinations of reverberating neural activity and neuromodulation, and demonstrate how whole-brain imaging can be used to discover loci underlying flexible behavior.

Organized by

Saikat Ray / Michael Brecht