Brain alignment of reasoning and action representations from vision-language and action models during naturalistic gameplay

Understanding how humans and artificial intelligence systems predict and plan by interacting with their environment is a fundamental challenge at the intersection of neuroscience and machine learning. Most brain-encoding studies focus on aligning artificial models with brain activity during language comprehension or passive visual processing, while interactive brain alignment studies have to date been largely limited to reinforcement-learning (RL) agents and theory-based models. To address this gap, we study brain alignment of representative models from two foundation-model types, namely vision-language models (VLMs) and large-action models (LAMs), using fMRI recordings from participants playing naturalistic Atari-style video games. Specifically, we examine how action-focused and reasoning-focused prompts shape the models' internal representations and their alignment with fMRI brain activity. First, we find that both VLMs and LAMs achieve significantly higher voxel-wise encoding performance than RL baselines, with the advantage holding even under matched feature dimensionality. Second, compared to a no-prompt baseline, prompt-driven gains are larger in higher-order frontal-parietal and motor-planning regions than in early visual cortex, roughly 2-2.5× when averaged over region-of-interest (ROI) groups, although individual regions are heterogeneous. Third, variance partitioning reveals a qualitatively different representational organization. VLM representations are prompt-symmetric (12.4% unique action vs. 9.5% unique reasoning), whereas LAM representations are action-dominant (25.6% unique action vs.-8.2% unique reasoning), with the asymmetry strongest in frontal-motor cortex. Together, these results associate action specialization with distinct cortical alignment patterns in multimodal game-state representations, revealing differences hidden by similar prediction accuracy.