A behavioral face preference deficit in a monkey with an incomplete face patch system

ABSTRACT Primates are experts in face perception and naturally show a preference for faces under free‐viewing conditions. The primate ventral stream is characterized by a network of face patches that selectively responds to faces, but it remains uncertain how important such parcellation is for face perception. Here we investigated free‐viewing behavior in a female monkey who naturally lacks fMRI‐defined posterior and middle lateral face patches. We presented a series of content‐rich images of scenes that included faces or other objects to that monkey during a free‐viewing task and tested a group of 10 control monkeys on the same task for comparison. We found that, compared to controls, the monkey with missing face patches showed a marked reduction of face viewing preference that was most pronounced for the first few fixations. In addition, her gaze fixation patterns were substantially distinct from those of controls, especially for pictures with a face. These data demonstrate an association between the clustering of neurons in face selective patches and a behavioral bias for faces in natural images. HIGHLIGHTSMonkey D naturally lacks fMRI‐defined posterior and middle lateral face patches.Face selective neurons didn't cluster in her middle lateral superior temporal sulcus.She showed a reduced face bias when free‐viewing content‐rich images with faces.Her fixation patterns were distinct from controls, especially for images with faces.

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

[2]  Margaret S. Livingstone,et al.  Seeing faces is necessary for face-patch formation , 2017, Nature Neuroscience.

[3]  Krista A. Ehinger,et al.  SUN database: Large-scale scene recognition from abbey to zoo , 2010, 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition.

[4]  Doris Y. Tsao,et al.  Anatomical Connections of the Functionally Defined “Face Patches” in the Macaque Monkey , 2016, Neuron.

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

[6]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[7]  Beatriz Luna,et al.  Location, Location, Location: Alterations in the Functional Topography of Face- but not Object- or Place-Related Cortex in Adolescents with Autism , 2009, Front. Hum. Neurosci..

[8]  K. Nakayama,et al.  Face detection in normal and prosopagnosic individuals. , 2008, Journal of neuropsychology.

[9]  Christopher F. Chabris,et al.  Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces , 2004, NeuroImage.

[10]  Lynn C. Robertson,et al.  Too Many Trees to See the Forest: Performance, Event-related Potential, and Functional Magnetic Resonance Imaging Manifestations of Integrative Congenital Prosopagnosia , 2007, Journal of Cognitive Neuroscience.

[11]  David A. Leopold,et al.  Face Pareidolia in the Rhesus Monkey , 2017, Current Biology.

[12]  Kim M. Dalton,et al.  Gaze fixation and the neural circuitry of face processing in autism , 2005, Nature Neuroscience.

[13]  Sébastien M. Crouzet,et al.  Fast saccades toward faces: face detection in just 100 ms. , 2010, Journal of vision.

[14]  Y. Sugita.  Face perception in monkeys reared with no exposure to faces , 2008, Proceedings of the National Academy of Sciences.

[15]  R. Schultz.  Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area , 2005, International Journal of Developmental Neuroscience.

[16]  J. DiCarlo,et al.  Optogenetic and pharmacological suppression of spatial clusters of face neurons reveal their causal role in face gender discrimination , 2015, Proceedings of the National Academy of Sciences.

[17]  Aidan P. Murphy,et al.  Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys , 2018, Proceedings of the National Academy of Sciences.

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

[19]  Elias B. Issa,et al.  Neurophysiological Organization of the Middle Face Patch in Macaque Inferior Temporal Cortex , 2016, The Journal of Neuroscience.

[20]  Stephen V. Shepherd,et al.  Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta). , 2014, Social cognitive and affective neuroscience.

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

[22]  Nouchine Hadjikhani,et al.  Neural basis of prosopagnosia: An fMRI study , 2002, Human brain mapping.

[23]  Rufin Vogels,et al.  Face Repetition Probability Does Not Affect Repetition Suppression in Macaque Inferotemporal Cortex , 2018, The Journal of Neuroscience.

[24]  Doris Y. Tsao,et al.  Single-Unit Recordings in the Macaque Face Patch System Reveal Limitations of fMRI MVPA , 2015, The Journal of Neuroscience.

[25]  Johan Wagemans,et al.  Perceived Shape Similarity among Unfamiliar Objects and the Organization of the Human Object Vision Pathway , 2008, The Journal of Neuroscience.

[26]  Guo Jiahui,et al.  Developmental prosopagnosics have widespread selectivity reductions across category-selective visual cortex , 2018, Proceedings of the National Academy of Sciences.

[27]  Doris Y. Tsao,et al.  The effect of face patch microstimulation on perception of faces and objects , 2017, Nature Neuroscience.

[28]  Guy A. Orban,et al.  Fine-grained stimulus representations in body selective areas of human occipito-temporal cortex , 2014, NeuroImage.

[29]  Teresa K. Pegors,et al.  Experimental manipulation of face-evoked activity in the fusiform gyrus of individuals with autism , 2011, Social neuroscience.

[30]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[31]  Jan Drewes,et al.  Smaller Is Better: Drift in Gaze Measurements due to Pupil Dynamics , 2014, PloS one.

[32]  Galit Yovel,et al.  Face recognition systems in monkey and human: are they the same thing? , 2013, F1000prime reports.

[33]  A. Klin,et al.  Infant viewing of social scenes is under genetic control and atypical in autism , 2017, Nature.

[34]  Wilbert Zarco,et al.  A causal relationship between face-patch activity and face-detection behavior , 2017, eLife.

[35]  Daniel P. Kennedy,et al.  Atypical Visual Saliency in Autism Spectrum Disorder Quantified through Model-Based Eye Tracking , 2015, Neuron.

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

[37]  Mark H. Johnson,et al.  Newborns' preference for face-relevant stimuli: effects of contrast polarity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[38]  K. Grill-Spector,et al.  Autism and the development of face processing , 2006, Clinical Neuroscience Research.

[39]  Christof Koch,et al.  Predicting human gaze using low-level saliency combined with face detection , 2007, NIPS.

[40]  Sarah Bate,et al.  Eye-Movement Strategies in Developmental Prosopagnosia and “Super” Face Recognition , 2017, Quarterly journal of experimental psychology.

[41]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[42]  Ming Chen,et al.  Visual Motion Processing in Macaque V2. , 2016, Cell reports.

[43]  W. Freiwald,et al.  Face Processing Systems: From Neurons to Real-World Social Perception. , 2016, Annual review of neuroscience.

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

[45]  Peter Janssen,et al.  Effective Connectivity Reveals Largely Independent Parallel Networks of Face and Body Patches , 2016, Current Biology.

[46]  Justin L. Vincent,et al.  Development of the macaque face-patch system , 2017, Nature Communications.

[47]  Justin L. Vincent,et al.  Novel domain formation reveals proto-architecture in inferotemporal cortex , 2014, Nature Neuroscience.

[48]  R. Vogels,et al.  Neural Correlate of the Thatcher Face Illusion in a Monkey Face-Selective Patch , 2015, The Journal of Neuroscience.

[49]  G. Rhodes,et al.  A comparative view of face perception. , 2010, Journal of comparative psychology.

[50]  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.

[51]  Bevil R. Conway,et al.  Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques , 2016, The Journal of Neuroscience.

[52]  N. Logothetis,et al.  fMRI of the Face-Processing Network in the Ventral Temporal Lobe of Awake and Anesthetized Macaques , 2011, Neuron.

[53]  Randolph Blake,et al.  Pupil size dynamics during fixation impact the accuracy and precision of video-based gaze estimation , 2016, Vision Research.

[54]  G. Yovel,et al.  Hierarchical Processing of Face Viewpoint in Human Visual Cortex , 2012, The Journal of Neuroscience.

[55]  R. Vogels,et al.  The impact of orientation filtering on face-selective neurons in monkey inferior temporal cortex , 2016, Scientific Reports.

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

[57]  Ivo D. Popivanov,et al.  Probabilistic and Single-Subject Retinotopic Maps Reveal the Topographic Organization of Face Patches in the Macaque Cortex , 2014, The Journal of Neuroscience.