Face processing pattern under top-down perception: a functional MRI study

Although top-down perceptual process plays an important role in face processing, its neural substrate is still puzzling because the top-down stream is extracted difficultly from the activation pattern associated with contamination caused by bottom-up face perception input. In the present study, a novel paradigm of instructing participants to detect faces from pure noise images is employed, which could efficiently eliminate the interference of bottom-up face perception in topdown face processing. Analyzing the map of functional connectivity with right FFA analyzed by conventional Pearson's correlation, a possible face processing pattern induced by top-down perception can be obtained. Apart from the brain areas of bilateral fusiform gyrus (FG), left inferior occipital gyrus (IOG) and left superior temporal sulcus (STS), which are consistent with a core system in the distributed cortical network for face perception, activation induced by top-down face processing is also found in these regions that include the anterior cingulate gyrus (ACC), right oribitofrontal cortex (OFC), left precuneus, right parahippocampal cortex, left dorsolateral prefrontal cortex (DLPFC), right frontal pole, bilateral premotor cortex, left inferior parietal cortex and bilateral thalamus. The results indicate that making-decision, attention, episodic memory retrieving and contextual associative processing network cooperate with general face processing regions to process face information under top-down perception.

[1]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

[2]  K. Nakayama,et al.  RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA , 2000, Cognitive neuropsychology.

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

[4]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[5]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[6]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[7]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[9]  Timothy E. J. Behrens,et al.  Adaptive decision making and value in the anterior cingulate cortex , 2007, NeuroImage.

[10]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[11]  M. Bar,et al.  Top-down predictions in the cognitive brain , 2007, Brain and Cognition.

[12]  M. Bar,et al.  The parahippocampal cortex mediates spatial and nonspatial associations. , 2007, Cerebral cortex.

[13]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[14]  Marcia K. Johnson,et al.  A brief thought can modulate activity in extrastriate visual areas: Top-down effects of refreshing just-seen visual stimuli , 2007, NeuroImage.

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

[16]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

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

[18]  M. Tarr,et al.  FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise , 2000, Nature Neuroscience.

[19]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[20]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[21]  Tobias Egner,et al.  Cerebral Cortex doi:10.1093/cercor/bhi129 Mistaking a House for a Face: Neural Correlates of Misperception in Healthy Humans , 2005 .

[22]  Jie Tian,et al.  BRAIN IMAGING NEUROREPORT , 2007 .

[23]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[24]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Florin Dolcos,et al.  Attention-related activity during episodic memory retrieval: a cross-function fMRI study , 2003, Neuropsychologia.

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

[27]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[28]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[29]  P. Bennett,et al.  Deriving behavioural receptive fields for visually completed contours , 2000, Current Biology.

[30]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

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

[32]  R. Knight,et al.  Prefrontal modulation of visual processing in humans , 2000, Nature Neuroscience.

[33]  Pascal Mamassian,et al.  Internal surface representations approximated by reverse correlation , 2004, Vision Research.

[34]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[35]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[36]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[38]  M. Bar,et al.  Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition , 2007, The Journal of Neuroscience.

[39]  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.

[40]  Julie A Fiez,et al.  Functional dissociations within the inferior parietal cortex in verbal working memory , 2004, NeuroImage.

[41]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[42]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[43]  Probing the brain with DNA chips , 1999, Nature Neuroscience.

[44]  Y. Miyashita,et al.  Neural representation of visual objects: encoding and top-down activation , 2000, Current Opinion in Neurobiology.

[45]  A. Owen,et al.  Prefrontal cortical involvement in verbal encoding strategies , 2004, The European journal of neuroscience.

[46]  Moshe Bar,et al.  Famous faces activate contextual associations in the parahippocampal cortex. , 2008, Cerebral cortex.

[47]  Talma Hendler,et al.  Center–periphery organization of human object areas , 2001, Nature Neuroscience.

[48]  Leslie G. Ungerleider,et al.  Visual Imagery of Famous Faces: Effects of Memory and Attention Revealed by fMRI , 2002, NeuroImage.

[49]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[50]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[51]  Karl J. Friston,et al.  Where bottom-up meets top-down: neuronal interactions during perception and imagery. , 2004, Cerebral cortex.

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

[53]  M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[54]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  D L Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Medial Blockintemporal Blockinlobe Blockinactivation Blockinduring Blockinepisodic Encoding Blockinand Blockinretrieval: Blockina Blockinpet Blockinstudy , 2022 .

[56]  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.

[57]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.