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Fast periodic stimulation (FPS): a highly effective approach in fMRI brain mapping

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Abstract

Defining the neural basis of perceptual categorization in a rapidly changing natural environment with low-temporal resolution methods such as functional magnetic resonance imaging (fMRI) is challenging. Here, we present a novel fast periodic stimulation (FPS)-fMRI approach to define face-selective brain regions with natural images. Human observers are presented with a dynamic stream of widely variable natural object images alternating at a fast rate (6 images/s). Every 9 s, a short burst of variable face images contrasting with object images in pairs induces an objective face-selective neural response at 0.111 Hz. A model-free Fourier analysis achieves a twofold increase in signal-to-noise ratio compared to a conventional block-design approach with identical stimuli and scanning duration, allowing to derive a comprehensive map of face-selective areas in the ventral occipito-temporal cortex, including the anterior temporal lobe (ATL), in all individual brains. Critically, periodicity of the desired category contrast and random variability among widely diverse images effectively eliminates the contribution of low-level visual cues, and lead to the highest values (80–90%) of test–retest reliability in the spatial activation map yet reported in imaging higher level visual functions. FPS-fMRI opens a new avenue for understanding brain function with low-temporal resolution methods.

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Notes

  1. Given this ratio and the respective number of nonface images and face images, nonface images repeat more often during a run than face images (i.e., ~ 3 times per face image versus ~ 10 times per object image). Equating the number of repetitions here would require using about 600 object images. Alternatively, one could reduce the number of face images, but at the expense of generalizability. Importantly, human electrophysiological studies using this stimulation mode have shown the same face-selective response with face and nonface images being equated for repetition (e.g., Rossion et al. 2015; Jacques et al., 2016) or not (Retter and Rossion 2016). Most importantly, the latter study directly demonstrated that the face-selective response is immune to large variations in ratios between the number of presented face and nonface images (Retter and Rossion 2016).

  2. All the data analysis scripts in the current study are available upon request.

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Acknowledgements

We thank Valérie Goffaux, Corentin Jacques, Jacques Jonas, Kirsten Petras, and Talia Retter and two anonymous reviewers for their helpful comments on an earlier version of this paper. We also thank Talia Retter for editing the manuscript.

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Authors and Affiliations

  1. Psychological Sciences Research Institute (IPSY), Institute of Neuroscience (IoNS), University of Louvain, 10, Place Cardinal Mercier, 1348, Louvain-la-Neuve, Belgium

    Xiaoqing Gao, Francesco Gentile & Bruno Rossion

  2. Department of Cognitive Neuroscience, Maastricht Brain Imaging Center (M-BIC), Maastricht University, 6211 LK, Maastricht, The Netherlands

    Francesco Gentile

  3. Université de Lorraine - CHRU-Nancy, CNRS, CRAN, Service de Neurologie, F-54000, Nancy, France

    Bruno Rossion

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  1. Xiaoqing Gao
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Gao, X., Gentile, F. & Rossion, B. Fast periodic stimulation (FPS): a highly effective approach in fMRI brain mapping. Brain Struct Funct 223, 2433–2454 (2018). https://doi.org/10.1007/s00429-018-1630-4

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