Optimal anticipatory control as a theory of motor preparation: A thalamo-cortical circuit model

• Published in: Neuron (Cambridge, Mass.) Mass.), 2021-05, Vol.109 (9), p.1567-1581.e12
• Main Authors: Kao, Ta-Chu, Sadabadi, Mahdieh S., Hennequin, Guillaume
• Format: Article
• Language: English
• Subjects: Animals; Anticipation, Psychological - physiology; Basal ganglia; Cerebral Cortex - physiology; Cognitive ability; Control theory; Dynamical systems; Feedback; Haplorhini; Hypotheses; manifold; Models, Neurological; movement preparation; neural circuits; Neural Pathways - physiology; neural population dynamics; Neurons; nullspace; optimal control; Population; Psychomotor Performance - physiology; thalamo-cortical loop; Thalamus - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2021.03.009

Across a range of motor and cognitive tasks, cortical activity can be accurately described by low-dimensional dynamics unfolding from specific initial conditions on every trial. These “preparatory states” largely determine the subsequent evolution of both neural activity and behavior, and their importance raises questions regarding how they are, or ought to be, set. Here, we formulate motor preparation as optimal anticipatory control of future movements and show that the solution requires a form of internal feedback control of cortical circuit dynamics. In contrast to a simple feedforward strategy, feedback control enables fast movement preparation by selectively controlling the cortical state in the small subspace that matters for the upcoming movement. Feedback but not feedforward control explains the orthogonality between preparatory and movement activity observed in reaching monkeys. We propose a circuit model in which optimal preparatory control is implemented as a thalamo-cortical loop gated by the basal ganglia. •Motor preparation is formalized as optimal control of M1 population dynamics•Preparatory activity can vary in a large subspace without causing future motor errors•A thalamo-cortical loop implements the optimal feedback control (OFC) solution•OFC explains fast preparation and key features of monkey M1 activity during reaching Optimal control theory has successfully explained aspects of motor cortex activity during but not before movement. Kao et al. formalize movement preparation as optimal feedback control of cortex. They show that optimal preparation can be realized in a thalamo-cortical loop, enables fast preparation, and explains prominent features of pre-movement activity.