Learning temporal integration from internal feedback

There has been much focus on the mechanisms of temporal integration, but little on how circuits learn to integrate. In the adult oculomotor system, where a neural integrator maintains fixations, changes in integration dynamics can be driven by visual error signals. However, we show through dark-rearing experiments that visual inputs are not necessary for initial integrator development. We therefore propose a vision-independent learning mechanism whereby a recurrent network learns to integrate via a teaching signal formed by low-pass filtered feedback of its population activity. The key is the segregation of local recurrent inputs onto a dendritic compartment and teaching inputs onto a somatic compartment of an integrator neuron. Model instantiation for oculomotor control shows how a self-corrective teaching signal through the cerebellum can generate an integrator with both the dynamical and tuning properties necessary to drive eye muscles and maintain gaze angle. This bootstrap learning paradigm may be relevant for development and plasticity of temporal integration more generally. Highlights- A neuronal architecture that learns to integrate saccadic commands for eye position. - Learning is based on the recurrent dendritic prediction of somatic teaching signals. - Experiment and model show that no visual feedback is required for initial integrator learning. - Cerebellum is an internal teacher for motor nuclei and integrator population.