Communications Biology (Jul 2024)

Erroneous predictive coding across brain hierarchies in a non-human primate model of autism spectrum disorder

  • Zenas C. Chao,
  • Misako Komatsu,
  • Madoka Matsumoto,
  • Kazuki Iijima,
  • Keiko Nakagaki,
  • Noritaka Ichinohe

DOI
https://doi.org/10.1038/s42003-024-06545-3
Journal volume & issue
Vol. 7, no. 1
pp. 1 – 16

Abstract

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Abstract In autism spectrum disorder (ASD), atypical sensory experiences are often associated with irregularities in predictive coding, which proposes that the brain creates hierarchical sensory models via a bidirectional process of predictions and prediction errors. However, it remains unclear how these irregularities manifest across different functional hierarchies in the brain. To address this, we study a marmoset model of ASD induced by valproic acid (VPA) treatment. We record high-density electrocorticography (ECoG) during an auditory task with two layers of temporal control, and applied a quantitative model to quantify the integrity of predictive coding across two distinct hierarchies. Our results demonstrate a persistent pattern of sensory hypersensitivity and unstable predictions across two brain hierarchies in VPA-treated animals, and reveal the associated spatio-spectro-temporal neural signatures. Despite the regular occurrence of imprecise predictions in VPA-treated animals, we observe diverse configurations of underestimation or overestimation of sensory regularities within the hierarchies. Our results demonstrate the coexistence of the two primary Bayesian accounts of ASD: overly-precise sensory observations and weak prior beliefs, and offer a potential multi-layered biomarker for ASD, which could enhance our understanding of its diverse symptoms.