Abstract

Functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG) research have been influential in revealing the functional characteristics of category-selective responses in human ventral temporal cortex (VTC). One important, but unanswered, question is how these two types of measurements might be related with respect to the VTC. Here we examined which components of the ECoG signal correspond to the fMRI response by using a rare opportunity to measure both fMRI and ECoG responses from the same individuals to images of exemplars of various categories including faces, limbs, cars and houses. Our data reveal three key findings. First, we discovered that the coupling between fMRI and ECoG responses is frequency and time dependent. The strongest and most sustained correlation is observed between fMRI and high frequency broadband (HFB) ECoG responses (30–160hz). In contrast, the correlation between fMRI and ECoG signals in lower frequency bands is temporally transient, where the correlation is initially positive, but then tapers off or becomes negative. Second, we find that the strong and positive correlation between fMRI and ECoG signals in all frequency bands emerges rapidly around 100ms after stimulus onset, together with the onset of the first stimulus-driven neural signals in VTC. Third, we find that the spatial topology and representational structure of category-selectivity in VTC reflected in ECoG HFB responses mirrors the topology and structure observed with fMRI. These findings of a strong and rapid coupling between fMRI and HFB responses validate fMRI measurements of functional selectivity with recordings of direct neural activity and suggest that fMRI category-selective signals in VTC are associated with feed-forward neural processing.

Highlights

  • Humans rapidly and accurately categorize visual objects and scenes from very brief presentations (Grill-Spector & Kanwisher, 2005; Thorpe, Fize, & Marlot, 1996). This ability is thought to depend on neural computations performed along a hierarchy of cortical areas in the ventral visual stream extending from primary visual cortex to high-level visual regions in ventral temporal cortex (VTC) (Ungerleider & Mishkin, 1982)

  • We focus on ECoG measurements in electrodes located over VTC including the posterior portion of the inferior temporal sulcus (ITS), inferior temporal gyrus (ITG), lateral (LFG) and medial (MFG) fusiform gyrus, collateral sulcus (CoS), parahippocampal gyrus (PHG) and the anterior part of the lingual gyrus (LG)

  • In the second part of our study we directly compared functional magnetic resonance imaging (fMRI) and ECoG responses in each of our participants addressing three main questions: (1) What is the spatial correspondence between face- and house-selectivity measured with ECoG high frequency broadband (HFB) to that measured with fMRI? We focused on these categories as they generated selective responses in both ECoG and fMRI in most of our participants

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Summary

Introduction

Humans rapidly and accurately categorize visual objects and scenes from very brief presentations (Grill-Spector & Kanwisher, 2005; Thorpe, Fize, & Marlot, 1996). FMRI research discovered that focal regions in human VTC show higher responses to ecologically-relevant categories such as faces, bodyparts, and places compared to other stimuli (Epstein & Kanwisher, 1998; Kanwisher, McDermott, & Chun, 1997; McCarthy, Puce, Gore, & Allison, 1997; Peelen & Downing, 2005; Schwarzlose, Baker, & Kanwisher, 2005) and that these regions have a consistent spatial organization (topology) relative to the cortical folding and relative to each other (Nasr et al, 2011; Weiner et al, 2014; Weiner & Grill-Spector, 2010, 2013; Witthoft et al, 2014). These consistent spatial topologies in VTC can be captured in representational similarity analyses (Kriegeskorte, et al, 2008), manifesting as higher correlations among VTC distributed responses to images of the same category compared to images of different categories

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