Generative replay underlies compositional inference in the hippocampal-prefrontal circuit

Philipp Schwartenbeck; Alon Baram; Yunzhe Liu; Shirley Mark; Timothy Muller; Raymond Dolan; Matthew Botvinick; Zeb Kurth-Nelson; Timothy Behrens

doi:10.1016/j.cell.2023.09.004

Generative replay underlies compositional inference in the hippocampal-prefrontal circuit

Cell. 2023 Oct 26;186(22):4885-4897.e14. doi: 10.1016/j.cell.2023.09.004. Epub 2023 Oct 6.

Authors

Philipp Schwartenbeck¹, Alon Baram², Yunzhe Liu³, Shirley Mark⁴, Timothy Muller⁵, Raymond Dolan⁶, Matthew Botvinick⁷, Zeb Kurth-Nelson⁸, Timothy Behrens⁹

Affiliations

¹ University of Tübingen, Tübingen, Germany; Max Planck Institute for Biological Cybernetics, Tübingen, Baden-Württemberg, Germany; Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3AR, UK; Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK. Electronic address: pschwartenbeck@gmail.com.
² Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK.
³ State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China; Chinese Institute for Brain Research, Beijing, China.
⁴ Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3AR, UK.
⁵ Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK; Institute of Neurology, University College London, London WC1N 3BG, UK.
⁶ Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3AR, UK; State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China; Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK; Department of Psychiatry, Universitätsmedizin Berlin (Campus Charité Mitte), Berlin, Germany.
⁷ Google DeepMind, London, UK; Gatsby Computational Neuroscience Unit, University College London, London, UK.
⁸ Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK; Google DeepMind, London, UK.
⁹ Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3AR, UK; Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK; Sainsbury Wellcome Centre for Neural Circuits and Behaviour, UCL, London W1T 4JG, UK.

Abstract

Human reasoning depends on reusing pieces of information by putting them together in new ways. However, very little is known about how compositional computation is implemented in the brain. Here, we ask participants to solve a series of problems that each require constructing a whole from a set of elements. With fMRI, we find that representations of novel constructed objects in the frontal cortex and hippocampus are relational and compositional. With MEG, we find that replay assembles elements into compounds, with each replay sequence constituting a hypothesis about a possible configuration of elements. The content of sequences evolves as participants solve each puzzle, progressing from predictable to uncertain elements and gradually converging on the correct configuration. Together, these results suggest a computational bridge between apparently distinct functions of hippocampal-prefrontal circuitry and a role for generative replay in compositional inference and hypothesis testing.

Keywords: cognitive maps; compositional inference; flexible reasoning; neural replay; prefrontal-hippocampal circuit.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Frontal Lobe
Hippocampus* / physiology
Humans
Magnetic Resonance Imaging / methods
Neural Pathways
Prefrontal Cortex* / physiology

Abstract

Publication types

MeSH terms

Grants and funding