Encoding time in neural dynamic regimes with distinct computational tradeoffs
Authors: Zhou Shanglin , Masmanidis Sotiris C. , Buonomano Dean V. 
Published: July 2021

Converging evidence suggests the brain encodes time in time-varying patterns of neural activity, including neural sequences, ramping activity, and complex dynamics. Temporal tasks that require producing the same time-dependent output patterns may have distinct computational requirements in regard to the need to exhibit temporal scaling or generalize to novel contexts. It is not known how neural circuits can both encode time and satisfy distinct computational and generalization requirements, it is also not known whether similar patterns of neural activity at the population level can emerge from distinctly different network configurations. 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 dynamics for single intervals were associated with fundamentally different encoding strategies and network configurations. Critically, some regimes were better suited for generalization, categorical timing, or robustness to noise. Further analysis revealed different connection patterns underlying the different encoding strategies. Our results predict that apparently similar neural dynamic regimes at the population level can be produced through fundamentally different mechanisms—e.g., in regard to network connectivity and the role 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, categorical timing, 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.