Rapid event-related, BOLD fMRI, non-human primates (NHP): choose two out of three

Human functional magnetic resonance imaging (fMRI) typically employs the blood-oxygen-level-dependent (BOLD) contrast mechanism. In non-human primates (NHP), contrast enhancement is possible using monocrystalline iron-oxide nanoparticles (MION) contrast agent, which has a more temporally extended response function. However, using BOLD fMRI in NHP is desirable for interspecies comparison, and the BOLD signal’s faster response function promises to be beneficial for rapid event-related (rER) designs. Here, we used rER BOLD fMRI in macaque monkeys while viewing real-world images, and found visual responses and category selectivity consistent with previous studies. However, activity estimates were very noisy, suggesting that the lower contrast-to-noise ratio of BOLD, suboptimal behavioural performance, and motion artefacts, in combination, render rER BOLD fMRI challenging in NHP. Previous studies have shown that rER fMRI is possible in macaques with MION, despite MION’s prolonged response function. To understand this, we conducted simulations of the BOLD and MION response during rER, and found that no matter how fast the design, the greater amplitude of the MION response outweighs the contrast loss caused by greater temporal smoothing. We conclude that although any two of the three elements (rER, BOLD, NHP) have been shown to work well, the combination of all three is particularly challenging.

[1]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[2]  Peter M. Kaskan,et al.  Learned Value Shapes Responses to Objects in Frontal and Ventral Stream Networks in Macaque Monkeys , 2016, Cerebral cortex.

[3]  Doris Y. Tsao,et al.  The Code for Facial Identity in the Primate Brain , 2017, Cell.

[4]  Peter Janssen,et al.  Effector Specificity in Macaque Frontal and Parietal Cortex , 2015, The Journal of Neuroscience.

[5]  Wim Vanduffel,et al.  The Retinotopic Organization of Macaque Occipitotemporal Cortex Anterior to V4 and Caudoventral to the Middle Temporal (MT) Cluster , 2014, The Journal of Neuroscience.

[6]  Doris Y. Tsao,et al.  Mechanisms of face perception. , 2008, Annual review of neuroscience.

[7]  Guy A. Orban,et al.  Monkey Cortex through fMRI Glasses , 2014, Neuron.

[8]  Leslie G. Ungerleider,et al.  Intrinsic Structure of Visual Exemplar and Category Representations in Macaque Brain , 2013, The Journal of Neuroscience.

[9]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[10]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  R. Tootell,et al.  An anterior temporal face patch in human cortex, predicted by macaque maps , 2009, Proceedings of the National Academy of Sciences.

[12]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[13]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[14]  J. Diedrichsen,et al.  On the distribution of cross-validated Mahalanobis distances , 2016, 1607.01371.

[15]  N. Kanwisher,et al.  The Human Body , 2001 .

[16]  C. Gross,et al.  Representations of faces and body parts in macaque temporal cortex: a functional MRI study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Bolton K. H. Chau,et al.  The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change , 2018, Nature Neuroscience.

[18]  John W. Harwell,et al.  Cortical parcellations of the macaque monkey analyzed on surface-based atlases. , 2012, Cerebral cortex.

[19]  R. Goebel,et al.  Homology and Specificity of Natural Sound-Encoding in Human and Monkey Auditory Cortex. , 2018, Cerebral cortex.

[20]  Jonathan W. Peirce,et al.  PsychoPy—Psychophysics software in Python , 2007, Journal of Neuroscience Methods.

[21]  N. Kriegeskorte,et al.  Faciotopy—A face-feature map with face-like topology in the human occipital face area , 2015, Cortex.

[22]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

[23]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[24]  Wim Vanduffel,et al.  Retinotopy versus Face Selectivity in Macaque Visual Cortex , 2014, Journal of Cognitive Neuroscience.

[25]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[27]  Jörn Diedrichsen,et al.  Reliability of dissimilarity measures for multi-voxel pattern analysis , 2016, NeuroImage.

[28]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[29]  Doris Y. Tsao,et al.  Functional Compartmentalization and Viewpoint Generalization Within the Macaque Face-Processing System , 2010, Science.

[30]  Leslie G. Ungerleider,et al.  Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex , 2008, Proceedings of the National Academy of Sciences.

[31]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[32]  Matthew F.S. Rushworth,et al.  Contrasting Roles for Orbitofrontal Cortex and Amygdala in Credit Assignment and Learning in Macaques , 2015, Neuron.

[33]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[34]  Kevin Whittingstall,et al.  Functional magnetic resonance imaging of awake behaving macaques. , 2010, Methods.

[35]  W. Vanduffel,et al.  Covert Shifts of Spatial Attention in the Macaque Monkey , 2015, The Journal of Neuroscience.

[36]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[37]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[38]  R. Vogels,et al.  The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions. , 2015, Journal of neurophysiology.

[39]  C. Gross,et al.  Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. , 2009, Journal of neurophysiology.

[40]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[41]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[42]  W. Vanduffel,et al.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex , 2009, The Journal of Neuroscience.

[43]  Robert Desimone,et al.  Cortical Connections of Area V4 in the Macaque , 2008 .

[44]  Joseph B. Mandeville,et al.  Characterization of event-related designs using BOLD and IRON fMRI , 2006, NeuroImage.

[45]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[46]  R. Andersen,et al.  Space representation for eye movements is more contralateral in monkeys than in humans , 2010, Proceedings of the National Academy of Sciences.

[47]  Wim Vanduffel,et al.  Stimulus representations in body-selective regions of the macaque cortex assessed with event-related fMRI , 2012, NeuroImage.

[48]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[49]  Leslie G. Ungerleider,et al.  Object representations in the temporal cortex of monkeys and humans as revealed by functional magnetic resonance imaging. , 2009, Journal of neurophysiology.

[50]  A. Thiele,et al.  Merging functional and structural properties of the monkey auditory cortex , 2014, Front. Neurosci..

[51]  D. V. van Essen,et al.  Windows on the brain: the emerging role of atlases and databases in neuroscience , 2002, Current Opinion in Neurobiology.

[52]  Bolton K. H. Chau,et al.  Inverted activity patterns in ventromedial prefrontal cortex during value-guided decision-making in a less-is-more task , 2017, Nature Communications.

[53]  W. Vanduffel,et al.  Areal differences in depth cue integration between monkey and human , 2019, PLoS biology.

[54]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[55]  David C. Van Essen,et al.  Windows on the brain: the emerging role of atlases and databases in neuroscience , 2002, Current Opinion in Neurobiology.

[56]  Peter M. Kaskan,et al.  Gustatory responses in macaque monkeys revealed with fMRI: Comments on taste, taste preference, and internal state , 2019, NeuroImage.

[57]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.