Parametric control of flexible timing through low-dimensional neural manifolds

Abstract

Biological brains possess an unparalleled ability to adapt behavioral responses to changing stimuli and environments. How neural processes enable this capacity is a fundamental open question. Previous works have identified two candidate mechanisms: a low-dimensional organization of neural activity and a modulation by contextual inputs. We hypothesized that combining the two might facilitate generalization and adaptation in complex tasks. We tested this hypothesis in flexible timing tasks where dynamics play a key role. Examining trained recurrent neural networks, we found that confining the dynamics to a low-dimensional subspace allowed tonic inputs to parametrically control the overall input-output transform, enabling generalization to novel inputs and adaptation to changing conditions. Reverse-engineering and theoretical analyses demonstrated that this parametric control relies on a mechanism where tonic inputs modulate the dynamics along non-linear manifolds while preserving their geometry. Comparisons with data from behaving monkeys confirmed the behavioral and neural signatures of this mechanism.