Controlling Visually Guided Behavior by Holographic Recalling of Cortical Ensembles

Neurons in cortical circuits are often coactivated as ensembles, yet it is unclear whether ensembles play a functional role in behavior. Some ensemble neurons have pattern completion properties, triggering the entire ensemble when activated. Using two-photon holographic optogenetics in mouse primary visual cortex, we tested whether recalling ensembles by activating pattern completion neurons alters behavioral performance in a visual task. Disruption of behaviorally relevant ensembles by activation of non-selective neurons decreased performance, whereas activation of only two pattern completion neurons from behaviorally relevant ensembles improved performance, by reliably recalling the whole ensemble. Also, inappropriate behavioral choices were evoked by the mistaken activation of behaviorally relevant ensembles. Finally, in absence of visual stimuli, optogenetic activation of two pattern completion neurons could trigger behaviorally relevant ensembles and correct behavioral responses. Our results demonstrate a causal role of neuronal ensembles in a visually guided behavior and suggest that ensembles implement internal representations of perceptual states. [Display omitted] •Holographic optogenetics of pattern completion neurons recalls behavioral ensembles•Recalling stimulus-specific neuronal ensembles improves a learned behavior•Disrupting stimulus-specific ensembles degrades a learned behavior•Activating 2 pattern completion neurons without any visual stimulus triggers behavior The activation of a small set of pattern completion neurons via two-photon holographic optogenetics triggers neuronal ensembles that appear to be necessary and sufficient for behavior.