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Neural populations encode the sensory world imperfectly: their capacity is limited by the number of neurons, availability of metabolic and other biophysical resources, and intrinsic noise. The brain is presumably shaped by these limitations, improving efficiency by discarding some aspects of incoming sensory streams, while preferentially preserving commonly occurring, behaviorally-relevant information. Here we construct a stochastic recurrent neural circuit model that can learn efficient, task-specific sensory codes using a novel form of reward-modulated Hebbian synaptic plasticity. We illustrate the flexibility of the model by training an initially unstructured neural network to solve two different tasks: stimulus estimation, and stimulus discrimination. The network achieves high performance in both tasks by appropriately allocating resources and using its recurrent circuitry to best compensate for different levels of noise. We also show how the interaction between stimulus priors and task structure dictates the emergent network representations.
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Modeling and dissociation of intrinsic and input-driven neural population dynamics underlying behavior
Neural dynamics can reflect intrinsic dynamics or dynamic inputs, such as sensory inputs or inputs from other brain 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 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 an analytical learning method for linear dynamical models that simultaneously accounts for neural activity, behavior, and measured inputs. The method provides the 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 the task while other methods can be influenced by the 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 different subjects and 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.
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- Award ID(s):
- 2113271
- PAR ID:
- 10559870
- Publisher / Repository:
- PNAS
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 121
- Issue:
- 7
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2212887121
