Intra- and interhemispheric connectivity between face-selective regions in the human brain.

Neuroimaging studies have revealed a number of regions in the human brain that respond to faces. However, the way these regions interact is a matter of current debate. The aim of this study was to use functional MRI to define face-selective regions in the human brain and then determine how these regions interact in a large population of subjects (n = 72). We found consistent face selectivity in the core face regions of the occipital and temporal lobes: the fusiform face area (FFA), occipital face area (OFA), and superior temporal sulcus (STS). Face selectivity extended into the intraparietal sulcus (IPS), precuneus (PCu), superior colliculus (SC), amygdala (AMG), and inferior frontal gyrus (IFG). We found evidence for significant functional connectivity between the core face-selective regions, particularly between the OFA and FFA. However, we found that the covariation in activity between corresponding face regions in different hemispheres (e.g., right and left FFA) was higher than between different face regions in the same hemisphere (e.g., right OFA and right FFA). Although functional connectivity was evident between regions in the core and extended network, there were significant differences in the magnitude of the connectivity between regions. Activity in the OFA and FFA were most correlated with the IPS, PCu, and SC. In contrast, activity in the STS was most correlated with the AMG and IFG. Correlations between the extended regions suggest strong functional connectivity between the IPS, PCu, and SC. In contrast, the IFG was only correlated with the AMG. This study reveals that interhemispheric as well as intrahemispheric connections play an important role in face perception.

[1]  A. L. I︠A︡rbus Eye Movements and Vision , 1967 .

[2]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[3]  H Steinmetz,et al.  Correlational Imaging of Thalamocortical Coupling in the Primary Visual Pathway of the Human Brain , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[4]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[5]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[6]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[7]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

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

[9]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[10]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  D. Sparks,et al.  Conceptual issues related to the role of the superior colliculus in the control of gaze , 1999, Current Opinion in Neurobiology.

[12]  P S Goldman-Rakic,et al.  Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. , 1999, Cerebral cortex.

[13]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[14]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[15]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[16]  E. Halgren,et al.  LOCALISED FACE PROCESSING BY THE HUMAN PREFRONTAL CORTEX: STIMULATION-EVOKED HALLUCINATIONS OF FACES , 2000, Cognitive neuropsychology.

[17]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[18]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[19]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[20]  Dietmar Cordes,et al.  Role of the corpus callosum in functional connectivity. , 2003, AJNR. American journal of neuroradiology.

[21]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[22]  R. Dolan,et al.  fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. , 2004, Journal of neurophysiology.

[23]  Michelle Hampson,et al.  Changes in functional connectivity of human MT/V5 with visual motion input , 2004, Neuroreport.

[24]  Timothy J. Andrews,et al.  Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe , 2004, NeuroImage.

[25]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[26]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[27]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[28]  Kenneth F. Valyear,et al.  The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area , 2006, Neuropsychologia.

[29]  Yehezkel Yeshurun,et al.  Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation , 2006, NeuroImage.

[30]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[31]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[32]  A. Ishai,et al.  Effective connectivity within the distributed cortical network for face perception. , 2007, Cerebral cortex.

[33]  Doris Y. Tsao,et al.  Patches of face-selective cortex in the macaque frontal lobe , 2008, Nature Neuroscience.

[34]  Paul E. Downing,et al.  The Face Network: Overextended? (Comment on: “Let's face it: It's a cortical network” by Alumit Ishai) , 2008, NeuroImage.

[35]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

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

[37]  Timothy J. Andrews,et al.  An image-dependent representation of familiar and unfamiliar faces in the human ventral stream , 2009, Neuropsychologia.

[38]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[39]  Arno Villringer,et al.  Resting developments: a review of fMRI post-processing methodologies for spontaneous brain activity , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[40]  Marc G. Berman,et al.  Evaluating functional localizers: The case of the FFA , 2010, NeuroImage.

[41]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[42]  Jie Tian,et al.  Effective connectivities of cortical regions for top-down face processing: A Dynamic Causal Modeling study , 2010, Brain Research.

[43]  Tom Hartley,et al.  Selectivity for low-level features of objects in the human ventral stream , 2010, NeuroImage.

[44]  Kalanit Grill-Spector,et al.  Sparsely-distributed organization of face and limb activations in human ventral temporal cortex , 2010, NeuroImage.

[45]  Nicholas B. Turk-Browne,et al.  Face-Specific Resting Functional Connectivity between the Fusiform Gyrus and Posterior Superior Temporal Sulcus , 2010, Front. Hum. Neurosci..

[46]  Timothy J. Andrews,et al.  Internal and External Features of the Face Are Represented Holistically in Face-Selective Regions of Visual Cortex , 2010, The Journal of Neuroscience.

[47]  P. Downing,et al.  Human Neuroscience , 2022 .

[48]  Patrik Vuilleumier,et al.  Processing social aspects of human gaze: A combined fMRI-DTI study , 2011, NeuroImage.

[49]  Dimitri Van De Ville,et al.  White-Matter Connectivity between Face-Responsive Regions in the Human Brain , 2012 .

[50]  Marvin M Chun,et al.  Category-selective background connectivity in ventral visual cortex. , 2012, Cerebral cortex.