Modeling and dissociation of intrinsic and input-driven neural population dynamics underlying behavior

Abstract

Neural dynamics can reflect intrinsic dynamics or dynamic inputs, such as sensory inputs or inputs from other regions. To avoid misinterpreting temporally-structured inputs as intrinsic dynamics, dynamical models of neural activity should account for measured inputs. However, incorporating measured inputs remains elusive in joint dynamical modeling of neural-behavioral data, which is important for studying neural computations of a specific behavior. We first show how training dynamical models of neural activity while considering behavior but not input, or input but not behavior may lead to misinterpretations. We then develop a novel analytical learning method that simultaneously accounts for neural activity, behavior, and measured inputs. The method provides the new capability to prioritize the learning of intrinsic behaviorally relevant neural dynamics and dissociate them from both other intrinsic dynamics and measured input dynamics. In data from a simulated brain with fixed intrinsic dynamics that performs different tasks, the method correctly finds the same intrinsic dynamics regardless of task while other methods can be influenced by the change in task. In neural datasets from three subjects performing two different motor tasks with task instruction sensory inputs, the method reveals low-dimensional intrinsic neural dynamics that are missed by other methods and are more predictive of behavior and/or neural activity. The method also uniquely finds that the intrinsic behaviorally relevant neural dynamics are largely similar across the three subjects and two tasks whereas the overall neural dynamics are not. These input-driven dynamical models of neural-behavioral data can uncover intrinsic dynamics that may otherwise be missed.