Experience transforms crossmodal object representations in the anterior temporal lobes

Elife. 2024 Apr 22:13:e83382. doi: 10.7554/eLife.83382.

Abstract

Combining information from multiple senses is essential to object recognition, core to the ability to learn concepts, make new inferences, and generalize across distinct entities. Yet how the mind combines sensory input into coherent crossmodal representations - the crossmodal binding problem - remains poorly understood. Here, we applied multi-echo fMRI across a 4-day paradigm, in which participants learned three-dimensional crossmodal representations created from well-characterized unimodal visual shape and sound features. Our novel paradigm decoupled the learned crossmodal object representations from their baseline unimodal shapes and sounds, thus allowing us to track the emergence of crossmodal object representations as they were learned by healthy adults. Critically, we found that two anterior temporal lobe structures - temporal pole and perirhinal cortex - differentiated learned from non-learned crossmodal objects, even when controlling for the unimodal features that composed those objects. These results provide evidence for integrated crossmodal object representations in the anterior temporal lobes that were different from the representations for the unimodal features. Furthermore, we found that perirhinal cortex representations were by default biased toward visual shape, but this initial visual bias was attenuated by crossmodal learning. Thus, crossmodal learning transformed perirhinal representations such that they were no longer predominantly grounded in the visual modality, which may be a mechanism by which object concepts gain their abstraction.

Keywords: concept learning; crossmodal binding problem; crossmodal object representations; human; integrative coding; multi-echo fMRI; neuroscience; unimodal features.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation
  • Adult
  • Auditory Perception / physiology
  • Brain Mapping
  • Female
  • Humans
  • Learning / physiology
  • Magnetic Resonance Imaging*
  • Male
  • Perirhinal Cortex / physiology
  • Photic Stimulation
  • Temporal Lobe* / diagnostic imaging
  • Temporal Lobe* / physiology
  • Visual Perception / physiology
  • Young Adult