Model-based spatial navigation in the hippocampus-ventral striatum circuit: A computational analysis

PLoS Comput Biol. 2018 Sep 17;14(9):e1006316. doi: 10.1371/journal.pcbi.1006316. eCollection 2018 Sep.

Abstract

While the neurobiology of simple and habitual choices is relatively well known, our current understanding of goal-directed choices and planning in the brain is still limited. Theoretical work suggests that goal-directed computations can be productively associated to model-based (reinforcement learning) computations, yet a detailed mapping between computational processes and neuronal circuits remains to be fully established. Here we report a computational analysis that aligns Bayesian nonparametrics and model-based reinforcement learning (MB-RL) to the functioning of the hippocampus (HC) and the ventral striatum (vStr)-a neuronal circuit that increasingly recognized to be an appropriate model system to understand goal-directed (spatial) decisions and planning mechanisms in the brain. We test the MB-RL agent in a contextual conditioning task that depends on intact hippocampus and ventral striatal (shell) function and show that it solves the task while showing key behavioral and neuronal signatures of the HC-vStr circuit. Our simulations also explore the benefits of biological forms of look-ahead prediction (forward sweeps) during both learning and control. This article thus contributes to fill the gap between our current understanding of computational algorithms and biological realizations of (model-based) reinforcement learning.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Animals
  • Bayes Theorem
  • Behavior, Animal
  • Brain / physiology*
  • Brain Mapping
  • Computer Simulation
  • Conditioning, Classical
  • Decision Making / physiology
  • Hippocampus / physiology*
  • Humans
  • Learning / physiology
  • Machine Learning
  • Maze Learning
  • Medical Informatics
  • Mice
  • Neurobiology
  • Reinforcement, Psychology
  • Software
  • Spatial Navigation*
  • Ventral Striatum / physiology*

Grants and funding

This research has received funding from the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 785907 (Human Brain Project SGA2 to GP and CP), the European Commission's Seventh Framework Programme (PIEF-GA- 2013-622882 to IS), and the Human Frontier Science Program (grant no. RGY0088/2014 to GP). The GEFORCE Titan GPU card used for this research was donated by the NVIDIA Corp. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.