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Published in: Brain Structure and Function 5/2018

01-06-2018 | Original Article

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

Authors: Xiaoqing Gao, Francesco Gentile, Bruno Rossion

Published in: Brain Structure and Function | Issue 5/2018

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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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Footnotes
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.
 
Literature
go back to reference Aguirre GK, D’Esposito M (1999) Experimental design for brain fMRI. Functional MRI. In: Moonen CTW, Bandettini PA (eds) Functional MRI. Springer, Berlin, pp 369–380 Aguirre GK, D’Esposito M (1999) Experimental design for brain fMRI. Functional MRI. In: Moonen CTW, Bandettini PA (eds) Functional MRI. Springer, Berlin, pp 369–380
go back to reference Amunts K, Zilles K (2015) Architectonic mapping of the human brain beyond Brodmann. Neuron 88:1086–1107PubMedCrossRef Amunts K, Zilles K (2015) Architectonic mapping of the human brain beyond Brodmann. Neuron 88:1086–1107PubMedCrossRef
go back to reference Andrews TJ, Watson DM, Rice GE, Hartley T (2015) Low-level properties of natural images predict topographic patterns of neural response in the ventral visual pathway. J Vis 15(7):3PubMedPubMedCentralCrossRef Andrews TJ, Watson DM, Rice GE, Hartley T (2015) Low-level properties of natural images predict topographic patterns of neural response in the ventral visual pathway. J Vis 15(7):3PubMedPubMedCentralCrossRef
go back to reference Avidan G, Tanzer M, Hadj-Bouziane F, Liu N, Ungerleider LG, Behrmann M (2014) Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. Cereb Cortex 24:1565–1578PubMedCrossRef Avidan G, Tanzer M, Hadj-Bouziane F, Liu N, Ungerleider LG, Behrmann M (2014) Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. Cereb Cortex 24:1565–1578PubMedCrossRef
go back to reference Axelrod V, Yovel G (2013) The challenge of localizing the anterior temporal face area: a possible solution. NeuroImage 81:371–380PubMedCrossRef Axelrod V, Yovel G (2013) The challenge of localizing the anterior temporal face area: a possible solution. NeuroImage 81:371–380PubMedCrossRef
go back to reference Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161–173PubMedCrossRef Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161–173PubMedCrossRef
go back to reference Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155PubMedCrossRef Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155PubMedCrossRef
go back to reference Benuzzi F, Pugnaghi M, Meletti S, Lui F, Serafini M, Baraldi P, Nichelli P (2007) Processing the socially relevant parts of faces. Brain Res Bull 74:344–356PubMedCrossRef Benuzzi F, Pugnaghi M, Meletti S, Lui F, Serafini M, Baraldi P, Nichelli P (2007) Processing the socially relevant parts of faces. Brain Res Bull 74:344–356PubMedCrossRef
go back to reference Berman MG, Park J, Gonzalez R, Polk TA, Gehrke A, Knaffla S, Jonides J (2010) Evaluating functional localizers: the case of the FFA. NeuroImage 50:56–71PubMedCrossRef Berman MG, Park J, Gonzalez R, Polk TA, Gehrke A, Knaffla S, Jonides J (2010) Evaluating functional localizers: the case of the FFA. NeuroImage 50:56–71PubMedCrossRef
go back to reference Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207–4221PubMedCrossRefPubMedCentral Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207–4221PubMedCrossRefPubMedCentral
go back to reference Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth JA, Leipzig Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth JA, Leipzig
go back to reference Busigny T, van Belle G, Jemel B, Hosein A, Joubert S, Rossion B (2014) Face-specific impairment in holistic perception following focal lesion of the right anterior temporal lobe. Neuropsychologia 56:312–333PubMedCrossRef Busigny T, van Belle G, Jemel B, Hosein A, Joubert S, Rossion B (2014) Face-specific impairment in holistic perception following focal lesion of the right anterior temporal lobe. Neuropsychologia 56:312–333PubMedCrossRef
go back to reference Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39:855–864PubMedCrossRef Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39:855–864PubMedCrossRef
go back to reference Buxton RB, Uludağ K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. NeuroImage 23:S220–S233PubMedCrossRef Buxton RB, Uludağ K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. NeuroImage 23:S220–S233PubMedCrossRef
go back to reference Calder AJ, Young AW (2005) Understanding the recognition of facial identity and facial expression. Nat Rev Neurosci 6:641–651PubMedCrossRef Calder AJ, Young AW (2005) Understanding the recognition of facial identity and facial expression. Nat Rev Neurosci 6:641–651PubMedCrossRef
go back to reference Chan AWY, Downing PE (2011) Faces and eyes in human lateral prefrontal cortex. Front Hum Neurosci 5(51):1–10 Chan AWY, Downing PE (2011) Faces and eyes in human lateral prefrontal cortex. Front Hum Neurosci 5(51):1–10
go back to reference Collins JA, Olson IR (2014) Beyond the FFA: the role of the ventral anterior temporal lobes in face processing. Neuropsychologia 61:65–79PubMedCrossRef Collins JA, Olson IR (2014) Beyond the FFA: the role of the ventral anterior temporal lobes in face processing. Neuropsychologia 61:65–79PubMedCrossRef
go back to reference D’Esposito M (2010) Why methods matter in the study of the biological basis of the mind: A behavioral neurologist’s perspective. In: Reuter-Lorenz PA, Baynes K, Mangun GR, Phelps EA (eds) The cognitive neuroscience of mind: a tribute to Michael S. Gazzaniga. MIT Press, Cambridge, pp 203–221CrossRef D’Esposito M (2010) Why methods matter in the study of the biological basis of the mind: A behavioral neurologist’s perspective. In: Reuter-Lorenz PA, Baynes K, Mangun GR, Phelps EA (eds) The cognitive neuroscience of mind: a tribute to Michael S. Gazzaniga. MIT Press, Cambridge, pp 203–221CrossRef
go back to reference de Heering A, Rossion B (2015) Rapid categorization of natural face images in the infant right hemisphere. eLife 4:1–14CrossRef de Heering A, Rossion B (2015) Rapid categorization of natural face images in the infant right hemisphere. eLife 4:1–14CrossRef
go back to reference Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage 53:1–15PubMedCrossRef Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage 53:1–15PubMedCrossRef
go back to reference Devlin JT, Russell RP, Davis MH, Price CJ, Wilson J, Moss HE, Tyler LK et al (2000) Susceptibility-induced loss of signal: comparing PET and fMRI on a semantic task. NeuroImage 11:589–600PubMedCrossRef Devlin JT, Russell RP, Davis MH, Price CJ, Wilson J, Moss HE, Tyler LK et al (2000) Susceptibility-induced loss of signal: comparing PET and fMRI on a semantic task. NeuroImage 11:589–600PubMedCrossRef
go back to reference Dormal G, Lepore F, Harissi-Dagher M, Albouy G, Bertone A, Rossion B, Collignon O (2015) Tracking the evolution of crossmodal plasticity and visual functions before and after sight restoration. J Neurophysiol 113:1727–1742PubMedCrossRef Dormal G, Lepore F, Harissi-Dagher M, Albouy G, Bertone A, Rossion B, Collignon O (2015) Tracking the evolution of crossmodal plasticity and visual functions before and after sight restoration. J Neurophysiol 113:1727–1742PubMedCrossRef
go back to reference Duchaine B, Yovel G (2015) A revised neural framework for face processing. Annu Rev Vis Sci 1:393–416PubMedCrossRef Duchaine B, Yovel G (2015) A revised neural framework for face processing. Annu Rev Vis Sci 1:393–416PubMedCrossRef
go back to reference Duncan KJ, Devlin JT (2011) Improving the reliability of functional localizers. NeuroImage 57(3):1022–1030CrossRef Duncan KJ, Devlin JT (2011) Improving the reliability of functional localizers. NeuroImage 57(3):1022–1030CrossRef
go back to reference Duncan KJ, Pattamadilok C, Knierim I, Devlin JT (2009) Consistency and variability in functional localisers. NeuroImage 46:1018–1026PubMedCrossRef Duncan KJ, Pattamadilok C, Knierim I, Devlin JT (2009) Consistency and variability in functional localisers. NeuroImage 46:1018–1026PubMedCrossRef
go back to reference Embleton KV, Haroon HA, Morris DM, Ralph MA, Parker GJ (2010) Distortion correction for diffusion-weighted MRI tractography and fMRI in the temporal lobes. Hum Brain Mapp 31:1570–1587PubMedCrossRefPubMedCentral Embleton KV, Haroon HA, Morris DM, Ralph MA, Parker GJ (2010) Distortion correction for diffusion-weighted MRI tractography and fMRI in the temporal lobes. Hum Brain Mapp 31:1570–1587PubMedCrossRefPubMedCentral
go back to reference Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192PubMedCrossRef Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192PubMedCrossRef
go back to reference Fischl B, Sereno MI, Tootell RBH, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284PubMedCrossRefPubMedCentral Fischl B, Sereno MI, Tootell RBH, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284PubMedCrossRefPubMedCentral
go back to reference Fox C, Moon S, Iaria G, Barton J (2009) The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. NeuroImage 44:569–580PubMedCrossRef Fox C, Moon S, Iaria G, Barton J (2009) The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. NeuroImage 44:569–580PubMedCrossRef
go back to reference Fox CJ, Hanif HM, Iaria G, Duchaine BC, Barton JJ (2011) Perceptual and anatomic patterns of selective deficits in facial identity and expression processing. Neuropsychologia 49:3188–3200PubMedCrossRef Fox CJ, Hanif HM, Iaria G, Duchaine BC, Barton JJ (2011) Perceptual and anatomic patterns of selective deficits in facial identity and expression processing. Neuropsychologia 49:3188–3200PubMedCrossRef
go back to reference Freud E, Ganel T, Shelef I, Hammer MD, Avidan G, Behrmann M (2017) Three-dimensional representations of objects in dorsal cortex are dissociable from those in ventral cortex. Cereb Cortex 27:422–434PubMedCrossRef Freud E, Ganel T, Shelef I, Hammer MD, Avidan G, Behrmann M (2017) Three-dimensional representations of objects in dorsal cortex are dissociable from those in ventral cortex. Cereb Cortex 27:422–434PubMedCrossRef
go back to reference Friston KJ, Price CJ, Fletcher P, Moore C, Frackowiak RS, Dolan RJ (1996) The trouble with cognitive subtraction. NeuroImage 4:97–104PubMedCrossRef Friston KJ, Price CJ, Fletcher P, Moore C, Frackowiak RS, Dolan RJ (1996) The trouble with cognitive subtraction. NeuroImage 4:97–104PubMedCrossRef
go back to reference Frost MA, Goebel R (2012) Measuring structural–functional correspondence: spatial variability of specialised brain regions after macro-anatomical alignment. NeuroImage 59:1369–1381PubMedCrossRef Frost MA, Goebel R (2012) Measuring structural–functional correspondence: spatial variability of specialised brain regions after macro-anatomical alignment. NeuroImage 59:1369–1381PubMedCrossRef
go back to reference Gauthier I, Tarr MJ, Moylan J, Skudlarski P, Gore JC, Anderson AW (2000) The fusiform “face area” is part of a network that processes faces at the individual level. J Cogn Neurosci 12:495–504PubMedCrossRef Gauthier I, Tarr MJ, Moylan J, Skudlarski P, Gore JC, Anderson AW (2000) The fusiform “face area” is part of a network that processes faces at the individual level. J Cogn Neurosci 12:495–504PubMedCrossRef
go back to reference Gentile F, Rossion B (2014) Temporal frequency tuning of cortical face-sensitive areas for individual face perception. NeuroImage 90:256–265PubMedCrossRef Gentile F, Rossion B (2014) Temporal frequency tuning of cortical face-sensitive areas for individual face perception. NeuroImage 90:256–265PubMedCrossRef
go back to reference Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, … Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178PubMedPubMedCentralCrossRef Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, … Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178PubMedPubMedCentralCrossRef
go back to reference Gobbini MI, Haxby JV (2006) Neural response to the visual familiarity of faces. Brain Res Bull 71:76–82PubMedCrossRef Gobbini MI, Haxby JV (2006) Neural response to the visual familiarity of faces. Brain Res Bull 71:76–82PubMedCrossRef
go back to reference Golarai G, Ghahremani DG, Whitfield-Gabrieli S, Reiss A, Eberhardt JL, Gabrieli JDE, Grill-Spector K (2007) Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat Neurosci 10:512–522PubMedPubMedCentralCrossRef Golarai G, Ghahremani DG, Whitfield-Gabrieli S, Reiss A, Eberhardt JL, Gabrieli JDE, Grill-Spector K (2007) Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat Neurosci 10:512–522PubMedPubMedCentralCrossRef
go back to reference Gomez J, Barnett MA, Natu V, Mezer A, Palomero-Gallagher N, Weiner KS, Grill-Spector K et al (2017) Microstructural proliferation in human cortex is coupled with the development of face processing. Science 355:68–71PubMedPubMedCentralCrossRef Gomez J, Barnett MA, Natu V, Mezer A, Palomero-Gallagher N, Weiner KS, Grill-Spector K et al (2017) Microstructural proliferation in human cortex is coupled with the development of face processing. Science 355:68–71PubMedPubMedCentralCrossRef
go back to reference Grill-Spector K, Weiner KS (2014) The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 15:536–548PubMedPubMedCentralCrossRef Grill-Spector K, Weiner KS (2014) The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 15:536–548PubMedPubMedCentralCrossRef
go back to reference Handwerker DA, Ollinger JM, D’Esposito M (2004) Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. NeuroImage 21:1639–1651PubMedCrossRef Handwerker DA, Ollinger JM, D’Esposito M (2004) Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. NeuroImage 21:1639–1651PubMedCrossRef
go back to reference Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223–233PubMedCrossRef Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4:223–233PubMedCrossRef
go back to reference Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293:2425–2430PubMedCrossRef Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293:2425–2430PubMedCrossRef
go back to reference Huth AG, Nishimoto S, Vu AT, Gallant JL (2012) A continuous semantic space describes the representation of thousands of object and action categories across the human brain. Neuron 76:1210–1224PubMedPubMedCentralCrossRef Huth AG, Nishimoto S, Vu AT, Gallant JL (2012) A continuous semantic space describes the representation of thousands of object and action categories across the human brain. Neuron 76:1210–1224PubMedPubMedCentralCrossRef
go back to reference Ishai A, Schmidt CF, Boesiger P (2005) Face perception is mediated by a distributed cortical network. Brain Res Bull 67:87–93PubMedCrossRef Ishai A, Schmidt CF, Boesiger P (2005) Face perception is mediated by a distributed cortical network. Brain Res Bull 67:87–93PubMedCrossRef
go back to reference Jokisch D, Jensen O (2007) Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. J Neurosci 27:3244–3251PubMedCrossRefPubMedCentral Jokisch D, Jensen O (2007) Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. J Neurosci 27:3244–3251PubMedCrossRefPubMedCentral
go back to reference Jonas J, Rossion B, Brissart H, Frismand S, Jacques C, Hossu G, Maillard L et al (2015) Beyond the core face-processing network: intracerebral stimulation of a face-selective area in the right anterior fusiform gyrus elicits transient prosopagnosia. Cortex 72:140–155PubMedCrossRef Jonas J, Rossion B, Brissart H, Frismand S, Jacques C, Hossu G, Maillard L et al (2015) Beyond the core face-processing network: intracerebral stimulation of a face-selective area in the right anterior fusiform gyrus elicits transient prosopagnosia. Cortex 72:140–155PubMedCrossRef
go back to reference Jonas J, Jacques C, Liu-Shuang J, Brissart H, Colnat-Coulbois S, Maillard L, Rossion B (2016) A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials. Proc Natl Acad Sci USA 113:E4088–E4097PubMedPubMedCentralCrossRef Jonas J, Jacques C, Liu-Shuang J, Brissart H, Colnat-Coulbois S, Maillard L, Rossion B (2016) A face-selective ventral occipito-temporal map of the human brain with intracerebral potentials. Proc Natl Acad Sci USA 113:E4088–E4097PubMedPubMedCentralCrossRef
go back to reference Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 7:4302–4311CrossRef Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 7:4302–4311CrossRef
go back to reference Kim J-J, Crespo-Facorro B, Andreasen NC, O’Leary DS, Zhang B, Harris G, Magnotta VA (2000) An MRI-based parcellation method for the temporal lobe. NeuroImage 11:271–288PubMedCrossRef Kim J-J, Crespo-Facorro B, Andreasen NC, O’Leary DS, Zhang B, Harris G, Magnotta VA (2000) An MRI-based parcellation method for the temporal lobe. NeuroImage 11:271–288PubMedCrossRef
go back to reference Koenig-Robert R, VanRullen R, Tsuchiya N (2015) Semantic wavelet-induced frequency-tagging (SWIFT) periodically activates category selective areas while steadily activating early visual areas. PLoS One 10:e0144858PubMedPubMedCentralCrossRef Koenig-Robert R, VanRullen R, Tsuchiya N (2015) Semantic wavelet-induced frequency-tagging (SWIFT) periodically activates category selective areas while steadily activating early visual areas. PLoS One 10:e0144858PubMedPubMedCentralCrossRef
go back to reference Kovacs G (2005) Electrophysiological correlates of visual adaptation to faces and body parts in humans. Cereb Cortex 16:742–753PubMedCrossRef Kovacs G (2005) Electrophysiological correlates of visual adaptation to faces and body parts in humans. Cereb Cortex 16:742–753PubMedCrossRef
go back to reference Kriegeskorte N, Formisano E, Sorger B, Goebel R (2007) Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc Natl Acad Sci USA 104:20600–20605PubMedPubMedCentralCrossRef Kriegeskorte N, Formisano E, Sorger B, Goebel R (2007) Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc Natl Acad Sci USA 104:20600–20605PubMedPubMedCentralCrossRef
go back to reference Krüger G, Glover GH (2001) Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magn Reson Med 46:631–637PubMedCrossRef Krüger G, Glover GH (2001) Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magn Reson Med 46:631–637PubMedCrossRef
go back to reference Lafer-sousa R, Conway BR, Kanwisher NG (2016) Color-biased regions of the ventral visual pathway lie between face- and place-selective regions in humans, as in macaques. J Neurosci 36:1682–1697PubMedPubMedCentralCrossRef Lafer-sousa R, Conway BR, Kanwisher NG (2016) Color-biased regions of the ventral visual pathway lie between face- and place-selective regions in humans, as in macaques. J Neurosci 36:1682–1697PubMedPubMedCentralCrossRef
go back to reference Lochy A, van Belle G, Rossion B (2015) A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation. Neuropsychologia 66:18–31PubMedCrossRef Lochy A, van Belle G, Rossion B (2015) A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation. Neuropsychologia 66:18–31PubMedCrossRef
go back to reference Loffler G, Yourganov G, Wilkinson F, Wilson HR (2005) fMRI evidence for the neural representation of faces. Nat Neurosci 8:1386–1391PubMedCrossRef Loffler G, Yourganov G, Wilkinson F, Wilson HR (2005) fMRI evidence for the neural representation of faces. Nat Neurosci 8:1386–1391PubMedCrossRef
go back to reference Maus B, van Breukelen GJP, Goebel R, Berger MPF (2010) Optimization of blocked designs in fMRI studies. Psychometrika 75:373–390CrossRef Maus B, van Breukelen GJP, Goebel R, Berger MPF (2010) Optimization of blocked designs in fMRI studies. Psychometrika 75:373–390CrossRef
go back to reference McCarthy G, Spicer M, Adrignolo A, Luby M, Gore JC, Allison T (1994) Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans. Hum Brain Mapp 2:234–243CrossRef McCarthy G, Spicer M, Adrignolo A, Luby M, Gore JC, Allison T (1994) Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans. Hum Brain Mapp 2:234–243CrossRef
go back to reference McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9:605–610PubMedCrossRef McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9:605–610PubMedCrossRef
go back to reference McKeefry D, Zeki S (1997) The position and topography of the human color centre as revealed by functional magnetic resonance imaging. Brain 120:2229–2242PubMedCrossRef McKeefry D, Zeki S (1997) The position and topography of the human color centre as revealed by functional magnetic resonance imaging. Brain 120:2229–2242PubMedCrossRef
go back to reference Murphy K, Bodurka J, Bandettini PA (2007) How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration. NeuroImage 34:565–574PubMedCrossRef Murphy K, Bodurka J, Bandettini PA (2007) How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration. NeuroImage 34:565–574PubMedCrossRef
go back to reference Nasr S, Tootell RB (2012) Role of fusiform and anterior temporal cortical areas in facial recognition. NeuroImage 63:1743–1753PubMedCrossRef Nasr S, Tootell RB (2012) Role of fusiform and anterior temporal cortical areas in facial recognition. NeuroImage 63:1743–1753PubMedCrossRef
go back to reference Nichols TE, Das S, Eickhoff SB, Evans AC, Glatard T, Hanke M …Yeo BTT (2017) Best practices in data analysis and sharing in neuroimaging using MRI. Nat Neurosci 20:299–303PubMedPubMedCentralCrossRef Nichols TE, Das S, Eickhoff SB, Evans AC, Glatard T, Hanke M …Yeo BTT (2017) Best practices in data analysis and sharing in neuroimaging using MRI. Nat Neurosci 20:299–303PubMedPubMedCentralCrossRef
go back to reference Norcia AM, Appelbaum LG, Ales JM, Cottereau B, Rossion B (2015) The steady-state visual evoked potential in vision research: a review. J Vis 15(6):4:1–46PubMedPubMedCentralCrossRef Norcia AM, Appelbaum LG, Ales JM, Cottereau B, Rossion B (2015) The steady-state visual evoked potential in vision research: a review. J Vis 15(6):4:1–46PubMedPubMedCentralCrossRef
go back to reference Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872PubMedPubMedCentralCrossRef Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872PubMedPubMedCentralCrossRef
go back to reference Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955PubMedPubMedCentralCrossRef Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955PubMedPubMedCentralCrossRef
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef
go back to reference Potter MC (2012) Recognition and memory for briefly presented scenes. Front Psychol 3:1–9 Potter MC (2012) Recognition and memory for briefly presented scenes. Front Psychol 3:1–9
go back to reference Puce A (1999) Electrophysiological studies of human face perception III: effects of top-down processing on face-specific potentials. Cereb Cortex 9:445–458PubMedCrossRef Puce A (1999) Electrophysiological studies of human face perception III: effects of top-down processing on face-specific potentials. Cereb Cortex 9:445–458PubMedCrossRef
go back to reference Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74:1192–1199PubMedCrossRef Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74:1192–1199PubMedCrossRef
go back to reference Rajimehr R, Young JC, Tootell RB (2009) An anterior temporal face patch in human cortex predicted by macaque maps. Proc Natl Acad Sci USA 106:1995–2000PubMedPubMedCentralCrossRef Rajimehr R, Young JC, Tootell RB (2009) An anterior temporal face patch in human cortex predicted by macaque maps. Proc Natl Acad Sci USA 106:1995–2000PubMedPubMedCentralCrossRef
go back to reference Regan D (1989) Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine. Elsevier, New York Regan D (1989) Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine. Elsevier, New York
go back to reference Retter TL, Rossion B (2016) Uncovering the neural magnitude and spatio-temporal dynamics of natural image categorization in a fast visual stream. Neuropsychologia 91:9–28PubMedCrossRef Retter TL, Rossion B (2016) Uncovering the neural magnitude and spatio-temporal dynamics of natural image categorization in a fast visual stream. Neuropsychologia 91:9–28PubMedCrossRef
go back to reference Rice GE, Watson DM, Hartley T, Andrews TJ (2014) Low-level image properties of visual objects predict patterns of neural response across category-selective regions of the ventral visual pathway. J Neurosci 34(26):8837–8844PubMedPubMedCentralCrossRef Rice GE, Watson DM, Hartley T, Andrews TJ (2014) Low-level image properties of visual objects predict patterns of neural response across category-selective regions of the ventral visual pathway. J Neurosci 34(26):8837–8844PubMedPubMedCentralCrossRef
go back to reference Rossion B, Boremanse A (2011) Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. J Vis 11(16):1–21 Rossion B, Boremanse A (2011) Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. J Vis 11(16):1–21
go back to reference Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126:2381–2395PubMedCrossRef Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126:2381–2395PubMedCrossRef
go back to reference Rossion B, Hanseeuw B, Dricot L (2012) Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis. Brain Cogn 79:138–157PubMedCrossRef Rossion B, Hanseeuw B, Dricot L (2012) Defining face perception areas in the human brain: a large-scale factorial fMRI face localizer analysis. Brain Cogn 79:138–157PubMedCrossRef
go back to reference Rossion B, Torfs K, Jacques C, Liu-Shuang J (2015) Fast periodic presentation of natural images reveals a robust face-selective electrophysiological response in the human brain. J Vis 15(18):1–18PubMed Rossion B, Torfs K, Jacques C, Liu-Shuang J (2015) Fast periodic presentation of natural images reveals a robust face-selective electrophysiological response in the human brain. J Vis 15(18):1–18PubMed
go back to reference Rossion B, Jacques C, Jonas J (2018) Mapping face categorization in the human ventral occipito-temporal cortex with direct neural intracranial recordings. Ann N Y Acad Sci Rossion B, Jacques C, Jonas J (2018) Mapping face categorization in the human ventral occipito-temporal cortex with direct neural intracranial recordings. Ann N Y Acad Sci
go back to reference Rousselet GA, Husk JS, Bennett PJ, Sekuler AB (2008) Time course and robustness of ERP object and face differences. J Vis 8(3):1–18CrossRefPubMed Rousselet GA, Husk JS, Bennett PJ, Sekuler AB (2008) Time course and robustness of ERP object and face differences. J Vis 8(3):1–18CrossRefPubMed
go back to reference Sadr J, Sinha P (2004) Object recognition and random image structure evolution. Cogn Sci 28:259–287CrossRef Sadr J, Sinha P (2004) Object recognition and random image structure evolution. Cogn Sci 28:259–287CrossRef
go back to reference Scherf KS, Behrmann M, Humphreys K, Luna B (2007) Visual category-selectivity for faces places and objects emerges along different developmental trajectories. Dev Sci 10:F15–F30PubMedCrossRef Scherf KS, Behrmann M, Humphreys K, Luna B (2007) Visual category-selectivity for faces places and objects emerges along different developmental trajectories. Dev Sci 10:F15–F30PubMedCrossRef
go back to reference Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268(5212):889–893PubMedCrossRef Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268(5212):889–893PubMedCrossRef
go back to reference Sergent J, Ohta S, MacDonald B (1992) Functional neuroanatomy of face and object processing. Brain 115:15–36PubMedCrossRef Sergent J, Ohta S, MacDonald B (1992) Functional neuroanatomy of face and object processing. Brain 115:15–36PubMedCrossRef
go back to reference Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216PubMedCrossRef Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216PubMedCrossRef
go back to reference Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Matthews PM et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:S208–S219PubMedCrossRef Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Matthews PM et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:S208–S219PubMedCrossRef
go back to reference Smith SM, Jenkinson M, Beckmann C, Miller K, Woolrich M (2007) Meaningful design and contrast estimability in FMRI. NeuroImage 34:127–136PubMedCrossRef Smith SM, Jenkinson M, Beckmann C, Miller K, Woolrich M (2007) Meaningful design and contrast estimability in FMRI. NeuroImage 34:127–136PubMedCrossRef
go back to reference Susilo T, Duchaine B (2013) Advances in developmental prosopagnosia research. Curr Opin Neurobiol 23:423–429PubMedCrossRef Susilo T, Duchaine B (2013) Advances in developmental prosopagnosia research. Curr Opin Neurobiol 23:423–429PubMedCrossRef
go back to reference Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381:520–522PubMedCrossRef Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381:520–522PubMedCrossRef
go back to reference Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Rosen BR et al (1995) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375:139–141PubMedCrossRef Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Rosen BR et al (1995) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375:139–141PubMedCrossRef
go back to reference Tuladhar AM, Huurne N, ter Schoffelen JM, Maris E, Oostenveld R, Jensen O (2007) Parieto-occipital sources account for the increase in alpha activity with working memory load. Hum Brain Mapp 28:785–792PubMedCrossRefPubMedCentral Tuladhar AM, Huurne N, ter Schoffelen JM, Maris E, Oostenveld R, Jensen O (2007) Parieto-occipital sources account for the increase in alpha activity with working memory load. Hum Brain Mapp 28:785–792PubMedCrossRefPubMedCentral
go back to reference VanRullen R (2006) On second glance: still no high-level pop-out effect for faces. Vis Res 46:3017–3027PubMedCrossRef VanRullen R (2006) On second glance: still no high-level pop-out effect for faces. Vis Res 46:3017–3027PubMedCrossRef
go back to reference Visser M, Embleton KV, Jefferies E, Parker GJ, Ralph MA (2010) The inferior, anterior temporal lobes and semantic memory clarified: novel evidence from distortion-corrected fMRI. Neuropsychologia 48:1689–1696PubMedCrossRef Visser M, Embleton KV, Jefferies E, Parker GJ, Ralph MA (2010) The inferior, anterior temporal lobes and semantic memory clarified: novel evidence from distortion-corrected fMRI. Neuropsychologia 48:1689–1696PubMedCrossRef
go back to reference Winawer J, Witthoft N (2015) Human V4 and ventral occipital retinotopic maps. Vis Neurosci 32:(E020) Winawer J, Witthoft N (2015) Human V4 and ventral occipital retinotopic maps. Vis Neurosci 32:(E020)
go back to reference Wang Y-F, Liu F, Long Z-L, Duan X-J, Cui Q, Yan JH, Chen H-F (2014) Steady-state BOLD response modulates low frequency neural oscillations. Sci Rep 4(7376):1–7 Wang Y-F, Liu F, Long Z-L, Duan X-J, Cui Q, Yan JH, Chen H-F (2014) Steady-state BOLD response modulates low frequency neural oscillations. Sci Rep 4(7376):1–7
go back to reference Wang Y-F, Dai G-S, Liu F, Long Z-L, Yan JH, Chen H-F (2015) Steady-state BOLD response to higher-order cognition modulates low-frequency neural oscillations. J Cogn Neurosci 27:2406–2415PubMedCrossRef Wang Y-F, Dai G-S, Liu F, Long Z-L, Yan JH, Chen H-F (2015) Steady-state BOLD response to higher-order cognition modulates low-frequency neural oscillations. J Cogn Neurosci 27:2406–2415PubMedCrossRef
go back to reference Weiner KS, Grill-Spector K (2010) Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. NeuroImage 52:1559–1573PubMedCrossRef Weiner KS, Grill-Spector K (2010) Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. NeuroImage 52:1559–1573PubMedCrossRef
go back to reference Weiner KS, Jonas J, Gomez J, Maillard L, Brissart H, Hossu G, Rossion B et al (2016) The face-processing network is resilient to focal resection of human visual cortex. J Neurosci 36:8425–8440PubMedPubMedCentralCrossRef Weiner KS, Jonas J, Gomez J, Maillard L, Brissart H, Hossu G, Rossion B et al (2016) The face-processing network is resilient to focal resection of human visual cortex. J Neurosci 36:8425–8440PubMedPubMedCentralCrossRef
go back to reference Worsley KJ, Marrett S, Neelin P, Evans AC (1996) Searching scale space for activation in PET images. Hum Brain Mapp 4:74–90PubMedCrossRef Worsley KJ, Marrett S, Neelin P, Evans AC (1996) Searching scale space for activation in PET images. Hum Brain Mapp 4:74–90PubMedCrossRef
go back to reference Yang H, Susilo T, Duchaine B (2016) The anterior temporal face area contains invariant representations of face identity that can persist despite the loss of right FFA and OFA. Cereb Cortex 26:1096–1107PubMedCrossRef Yang H, Susilo T, Duchaine B (2016) The anterior temporal face area contains invariant representations of face identity that can persist despite the loss of right FFA and OFA. Cereb Cortex 26:1096–1107PubMedCrossRef
go back to reference Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Sci 6:37–46PubMedCrossRef Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Sci 6:37–46PubMedCrossRef
go back to reference Zhen Z, Yang Z, Huang L, Kong X, Wang X, Dang X, Huang Y, Song Y, Liu J (2015) Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. NeuroImage 113:13–25PubMedCrossRef Zhen Z, Yang Z, Huang L, Kong X, Wang X, Dang X, Huang Y, Song Y, Liu J (2015) Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. NeuroImage 113:13–25PubMedCrossRef
Metadata
Title
Fast periodic stimulation (FPS): a highly effective approach in fMRI brain mapping
Authors
Xiaoqing Gao
Francesco Gentile
Bruno Rossion
Publication date
01-06-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 5/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1630-4

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