The Ventral Visual Pathway Represents Animal Appearance over Animacy, Unlike Human Behavior and Deep Neural Networks

J Neurosci. 2019 Aug 14;39(33):6513-6525. doi: 10.1523/JNEUROSCI.1714-18.2019. Epub 2019 Jun 13.


Recent studies showed agreement between how the human brain and neural networks represent objects, suggesting that we might start to understand the underlying computations. However, we know that the human brain is prone to biases at many perceptual and cognitive levels, often shaped by learning history and evolutionary constraints. Here, we explore one such perceptual phenomenon, perceiving animacy, and use the performance of neural networks as a benchmark. We performed an fMRI study that dissociated object appearance (what an object looks like) from object category (animate or inanimate) by constructing a stimulus set that includes animate objects (e.g., a cow), typical inanimate objects (e.g., a mug), and, crucially, inanimate objects that look like the animate objects (e.g., a cow mug). Behavioral judgments and deep neural networks categorized images mainly by animacy, setting all objects (lookalike and inanimate) apart from the animate ones. In contrast, activity patterns in ventral occipitotemporal cortex (VTC) were better explained by object appearance: animals and lookalikes were similarly represented and separated from the inanimate objects. Furthermore, the appearance of an object interfered with proper object identification, such as failing to signal that a cow mug is a mug. The preference in VTC to represent a lookalike as animate was even present when participants performed a task requiring them to report the lookalikes as inanimate. In conclusion, VTC representations, in contrast to neural networks, fail to represent objects when visual appearance is dissociated from animacy, probably due to a preferred processing of visual features typical of animate objects.SIGNIFICANCE STATEMENT How does the brain represent objects that we perceive around us? Recent advances in artificial intelligence have suggested that object categorization and its neural correlates have now been approximated by neural networks. Here, we show that neural networks can predict animacy according to human behavior but do not explain visual cortex representations. In ventral occipitotemporal cortex, neural activity patterns were strongly biased toward object appearance, to the extent that objects with visual features resembling animals were represented closely to real animals and separated from other objects from the same category. This organization that privileges animals and their features over objects might be the result of learning history and evolutionary constraints.

Keywords: MVPA; animacy; deep neural networks; fMRI; object representations; occipitotemporal cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Neural Networks, Computer*
  • Pattern Recognition, Visual / physiology*
  • Visual Cortex / physiology*
  • Visual Pathways / physiology*