A mechanistic theory of planning in prefrontal cortex

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Abstract
Planning is critical for adaptive behaviour in a changing world, because it lets us anticipate the future and adjust our actions accordingly. While prefrontal cortex is crucial for this process, it remains unknown how planning is implemented in neural circuits. Prefrontal representations were recently discovered in simpler sequence memory tasks, where different populations of neurons represent different future time points. We demonstrate that combining such representations with the ubiquitous principle of neural attractor dynamics allows circuits to solve much richer problems, including planning. This is achieved by embedding the environment structure directly in synaptic connections to implement an attractor network that infers desirable futures. The resulting ‘spacetime attractor’ excels at planning in challenging tasks known to depend on the prefrontal cortex. Recurrent neural networks trained by gradient descent on such tasks learn a solution that precisely recapitulates the spacetime attractor – in representation, in dynamics, and in connectivity. Analyses of networks trained across different environment structures reveal a generalisation mechanism that rapidly reconfigures the world model used for planning, without the need for synaptic plasticity. The spacetime attractor is a testable mechanistic theory of planning. If true, it would provide a path towards detailed mechanistic understanding of how prefrontal cortex structures adaptive behaviour.
Funding Information
  • Wellcome Trust (10.35802/219525)
  • Wellcome Trust (10.35802/225926)
  • Wellcome Trust (Sainsbury Wellcome Centre's core 219627/Z/19/Z)
  • Gatsby Charitable Foundation (Sainsbury Wellcome Centre's core GAT3755)
  • Gatsby Charitable Foundation (The Gatsby Initiative for Brain Development and Psychiatry GAT3955)
  • The Jean Francois and Marie-Laure de Clermont Tonerre Foundation
  • The Oxford Clarendon Fund
  • Human Frontier Science Program (10.52044/HFSP.LT00402024-L.pc.gr.195051)
  • European Molecular Biology Organization (ALTF 651-2023)
  • Fondation Fyssen
  • Gatsby Charitable Foundation (GAT4058)
  • Simons Foundation (SCGB543039)
  • Royal Society (FDF\S2\251056)

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