Encoding time in neural dynamic regimes with distinct computational tradeoffs

Abstract

Converging evidence suggests the brain encodes time in dynamic patterns of neural activity, including neural sequences, ramping activity, and complex dynamics. Most temporal tasks, however, require more than just encoding time, and can have distinct computational requirements including the need to exhibit temporal scaling, generalize to novel contexts, or robustness to noise. It is not known how neural circuits can encode time and satisfy distinct computational requirements, nor is it known whether similar patterns of neural activity at the population level can exhibit dramatically different computational or generalization properties. To begin to answer these questions, we trained RNNs on two timing tasks based on behavioral studies. The tasks had different input structures but required producing identically timed output patterns. Using a novel framework we quantified whether RNNs encoded two intervals using either of three different timing strategies: scaling, absolute, or stimulus-specific dynamics. We found that similar neural dynamic patterns at the level of single intervals, could exhibit fundamentally different properties, including, generalization, the connectivity structure of the trained networks, and the contribution of excitatory and inhibitory neurons. Critically, depending on the task structure RNNs were better suited for generalization or robustness to noise. Further analysis revealed different connection patterns underlying the different regimes. Our results predict that apparently similar neural dynamic patterns at the population level (e.g., neural sequences) can exhibit fundamentally different computational properties in regards to their ability to generalize to novel stimuli and their robustness to noise—and that these differences are associated with differences in network connectivity and distinct contributions of excitatory and inhibitory neurons. We also predict that the task structure used in different experimental studies accounts for some of the experimentally observed variability in how networks encode time. Author summary The ability to tell time and anticipate when external events will occur are among the most fundamental computations the brain performs. Converging evidence suggests the brain encodes time through changing patterns of neural activity. Different temporal tasks, however, have distinct computational requirements, such as the need to flexibly scale temporal patterns or generalize to novel inputs. To understand how networks can encode time and satisfy different computational requirements we trained recurrent neural networks (RNNs) on two timing tasks that have previously been used in behavioral studies. Both tasks required producing identically timed output patterns. Using a novel framework to quantify how networks encode different intervals, we found that similar patterns of neural activity—neural sequences—were associated with fundamentally different underlying mechanisms, including the connectivity patterns of the RNNs. Critically, depending on the task the RNNs were trained on, they were better suited for generalization or robustness to noise. Our results predict that similar patterns of neural activity can be produced by distinct RNN configurations, which in turn have fundamentally different computational tradeoffs. Our results also predict that differences in task structure account for some of the experimentally observed variability in how networks encode time.