Abstract

A key question in cognitive neuroscience is how the brain combines low-level features processed in remote sensory cortices to represent meaningful multisensory objects in our everyday environment. Models of visual object processing typically assume a feedforward cascade through the hierarchically organized ventral stream. We contrasted this feedforward view with an alternate hypothesis in which object processing is viewed as an interactive, feedforward and feedback process. We found that higher-order regions in anterior temporal (AT) and inferior prefrontal cortex (IPC) performed audio-visual (AV) integration 100 ms earlier than a sensory-driven region in the posterior occipital (pO) cortex, and were modulated by semantic variables (congruency), from as early as 50–100 ms. We propose that the brain represents familiar and complex multisensory objects through early interactivity between higher-order and sensory-driven regions. This interactivity may underpin the enhanced behavioral performance reported for semantically congruent AV objects.

Highlights

  • To recognize a familiar object in our everyday environment, the brain effortlessly integrates inputs from different sensory modalities into a coherent meaningful representation

  • While multisensory integration responses have been consistently reported at numerous sites across the cortex, a key, unresolved question in cognitive neuroscience concerns the temporal mechanism that combines multisensory integration responses to familiar object features that occur across the brain into an object representation. fMRI studies have consistently reported audiovisual (AV) integration responses to complex stimuli in both auditory (A) and visual (V) sensory regions, and in higher-order anterior ventral regions

  • SOURCE MODELING ANALYSIS We analyzed the source-localized unimodal (A/V) responses for proof of principle that the superior temporal (ST) and posterior occipital (pO) regions were primarily driven by sensory processes, whereas the anterior temporal (AT) and inferior prefrontal cortex (IPC) regions were driven by higher-order processes

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Summary

Introduction

To recognize a familiar object in our everyday environment (e.g., an animal or a tool), the brain effortlessly integrates inputs from different sensory modalities into a coherent meaningful representation. AV responses to meaningful multisensory object stimuli have been reported in regions higher-up in the object processing hierarchy, including the lateral temporal (Beauchamp et al, 2004; Hein et al, 2007), anterior temporal (AT), and in particular the antero-medial temporal cortex (AMTC) (Taylor et al, 2006), prefrontal cortex (Laurienti et al, 2003), and inferior prefrontal cortex (IPC) (Hein et al, 2007) It remains unclear when AV integration responses in higher-order and sensory-driven regions interact, and whether integration responses from anterior ventral regions feed back to affect integration responses in posterior occipital (pO) regions from early stages of multisensory object processing. Studies on visual object recognition (Barceló et al, 2000; Bar et al, 2006) instead support an interactive feedforward and feedback (top–down) model of object recognition, whereby processes in higher-order regions influence those in sensory-driven regions from the earliest stages, prior to recognition, and before a fine-grained meaningful representation has been achieved (Lamme and Roelfsema, 2000; Bullier, 2001; Bar et al, 2006; Clarke et al, 2011)

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