Reproducing Human Motor Adaptation in Spiking Neural Simulation and known Synaptic Learning Rules

Abstract

Sensorimotor adaptation enables us to adjust our goal-oriented movements in response to external perturbations. These phenomena have been studied experimentally and computationally at the level of human and animals reaching movements, and have clear links to the cerebellum as evidenced by cerebellar lesions and neurodegeneration. Yet, despite our macroscopic understanding of the high-level computational mechanisms it is unclear how these are mapped and are implemented in the neural substrates of the cerebellum at a cellular-computational level. We present here a novel spiking neural circuit model of the sensorimotor system including a cerebellum which control physiological muscle models to reproduce behaviour experiments. Our cerebellar model is composed of spiking neuron populations reflecting cells in the cerebellar cortex and deep cerebellar nuclei, which generate motor correction to change behaviour in response to perturbations. The model proposes two learning mechanisms for adaptation: predictive learning and memory formation, which are implemented with synaptic updating rules. Our model is tested in a force-field sensorimotor adaptation task and successfully reproduce several phenomena arising from human adaptation, including well-known learning curves, aftereffects, savings and other multi-rate learning effects. This reveals the capability of our model to learn from perturbations and generate motor corrections while providing a bottom-up view for the neural basis of adaptation. Thus, it also shows the potential to predict how patients with specific types of cerebellar damage will perform in behavioural experiments. We explore this by in silico experiments where we selectively incapacitate selected cerebellar circuits of the model which generate and reproduce defined motor learning deficits. Author summaryA rich body of work in human motor neuroscience developed high-level computational theories of sensorimotor control, learning and adaptation. But there is a gap in understanding how this may be implemented and learn on the level of neurons, synapses and spikes. Conversely, studies of patients with cerebellar lesions or neurological disease highlight the essential role the cerebellum plays in our ability to perform motor learning. Yet, how these anatomical and molecular defects play out in terms of human movement have to date not been linked to a model that spans multiple level of biological organisation from neural circuits to reproducing human motor experiments. To address this gap, we present a spiking neuron of the sensorimotor system focused on the cerebellum, with which we can on the one side reproduce the high-level behaviour learning phenomena observed in healthy subjects, as well as quantitatively predicting the putative effects on human movement trajectories of cerebellar lesions implemented at the cellular level.