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Binding crossmodal object features in perirhinal cortex

  1. Kirsten I. Taylor * , † , ‡ ,
  2. Helen E. Moss *,
  3. Emmanuel A. Stamatakis * , § , and
  4. Lorraine K. Tyler * , §
  1. *Department of Experimental Psychology, University of Cambridge, Downing Street, Cambridge CB2 3EB, United Kingdom;
  2. †Memory Clinic–Neuropsychology Center, University Hospital Basel, Schanzenstrasse 55, CH-4031 Basel, Switzerland; and
  3. §Wolfson Brain Imaging Centre, University of Cambridge, Cambridge CB2 2QQ, United Kingdom

  1. Edited by Charles G. Gross, Princeton University, Princeton, NJ, and approved April 7, 2006 (received for review November 8, 2005)

Abstract

Knowledge of objects in the world is stored in our brains as rich, multimodal representations. Because the neural pathways that process this diverse sensory information are largely anatomically distinct, a fundamental challenge to cognitive neuroscience is to explain how the brain binds the different sensory features that comprise an object to form meaningful, multimodal object representations. Studies with nonhuman primates suggest that a structure at the culmination of the object recognition system (the perirhinal cortex) performs this critical function. In contrast, human neuroimaging studies implicate the posterior superior temporal sulcus (pSTS). The results of the functional MRI study reported here resolve this apparent discrepancy by demonstrating that both pSTS and the perirhinal cortex contribute to crossmodal binding in humans, but in different ways. Significantly, only perirhinal cortex activity is modulated by meaning variables (e.g., semantic congruency and semantic category), suggesting that these two regions play complementary functional roles, with pSTS acting as a presemantic, heteromodal region for crossmodal perceptual features, and perirhinal cortex integrating these features into higher-level conceptual representations. This interpretation is supported by the results of our behavioral study: Patients with lesions, including the perirhinal cortex, but not patients with damage restricted to frontal cortex, were impaired on the same crossmodal integration task, and their performance was significantly influenced by the same semantic factors, mirroring the functional MRI findings. These results integrate nonhuman and human primate research by providing converging evidence that human perirhinal cortex is also critically involved in processing meaningful aspects of multimodal object representations.

Footnotes

  • ‡To whom correspondence should be addressed. E-mail: ktaylor{at}csl.psychol.cam.ac.uk

  • ↵ Brett, M., Anton, J.-L., Valabregue, R. & Poline, J.-B. (2002) NeuroImage 16, S497 (abstr.).

  • Author contributions: K.I.T., H.E.M., E.A.S., and L.K.T. designed research; K.I.T. performed research; K.I.T., H.E.M., E.A.S., and L.K.T. analyzed data; and K.I.T., H.E.M., E.A.S., and L.K.T. wrote the paper.

  • Conflict of interest statement: No conflicts declared.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations:

    Abbreviations:

    fMRI,
    functional MRI;
    efMRI,
    event-related fMRI;
    HSE,
    herpes simplex encephalitis;
    LIFC,
    left inferior frontal cortex;
    MC,
    mature control;
    MTG,
    middle temporal gyrus;
    ns,
    not significant;
    pSTS,
    posterior superior temporal sulcus.

  • Freely available online through the PNAS open access option.

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