The effect of face patch microstimulation on perception of faces and objects

What is the range of stimuli encoded by face-selective regions of the brain? We asked how electrical microstimulation of face patches in macaque inferotemporal cortex affects perception of faces and objects. We found that microstimulation strongly distorted face percepts and that this effect depended on precise targeting to the center of face patches. While microstimulation had no effect on the percept of many non-face objects, it did affect the percept of some, including non-face objects whose shape is consistent with a face (for example, apples) as well as somewhat facelike abstract images (for example, cartoon houses). Microstimulation even perturbed the percept of certain objects that did not activate the stimulated face patch at all. Overall, these results indicate that representation of facial identity is localized to face patches, but activity in these patches can also affect perception of face-compatible non-face objects, including objects normally represented in other parts of inferotemporal cortex.

[1]  R. Fisher.  On the Interpretation of χ2 from Contingency Tables, and the Calculation of P , 2018, Journal of the Royal Statistical Society Series A (Statistics in Society).

[2]  C. M. Mooney.  Age in the development of closure ability in children. , 1957, Canadian journal of psychology.

[3]  J. Kugler,et al.  Subjective Light Pattern Spectroscopy in the Encephalographic Frequency Range , 1959, Nature.

[4]  W. Penfield,et al.  THE BRAIN'S RECORD OF AUDITORY AND VISUAL EXPERIENCE. A FINAL SUMMARY AND DISCUSSION. , 1963, Brain : a journal of neurology.

[5]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[6]  G. Brindley,et al.  The sensations produced by electrical stimulation of the visual cortex , 1968, The Journal of physiology.

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

[8]  A. Mikami,et al.  Inferotemporal neuron activities and color discrimination with delay , 1980, Brain Research.

[9]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[11]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.

[13]  G. Orban,et al.  Does Practice in Orientation Discrimination Lead to Changes in the Response Properties of Macaque Inferior Temporal Neurons? , 1994, The European journal of neuroscience.

[14]  G. Orban,et al.  Activity of inferior temporal neurons during orientation discrimination with successively presented gratings. , 1994, Journal of neurophysiology.

[15]  T. Allison,et al.  Face recognition in human extrastriate cortex. , 1994, Journal of neurophysiology.

[16]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[17]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

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

[19]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[20]  Talma Hendler,et al.  Eccentricity Bias as an Organizing Principle for Human High-Order Object Areas , 2002, Neuron.

[21]  G. Orban,et al.  Search for color 'center(s)' in macaque visual cortex. , 2004, Cerebral cortex.

[22]  E. Rolls,et al.  Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks , 2004, Experimental Brain Research.

[23]  Arnold W. M. Smeulders,et al.  The Amsterdam Library of Object Images , 2004, International Journal of Computer Vision.

[24]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

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

[26]  R. Kiani,et al.  Microstimulation of inferotemporal cortex influences face categorization , 2006, Nature.

[27]  Nancy Kanwisher,et al.  Privileged coding of convex shapes in human object-selective cortex. , 2008, Journal of neurophysiology.

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

[29]  Doris Y. Tsao,et al.  A face feature space in the macaque temporal lobe , 2009, Nature Neuroscience.

[30]  Iwan C. Pritchard,et al.  Animate and inanimate objects in human visual cortex: Evidence for task-independent category effects , 2009, Neuropsychologia.

[31]  R. Fisher.  On the Interpretation of χ2 from Contingency Tables, and the Calculation of P , 2010 .

[32]  R. Vogels,et al.  Contribution of Inferior Temporal and Posterior Parietal Activity to Three-Dimensional Shape Perception , 2010, Current Biology.

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

[34]  Doris Y. Tsao,et al.  MR-guided stereotactic navigation , 2012, Journal of Neuroscience Methods.

[35]  Doris Y. Tsao,et al.  What Makes a Cell Face Selective? The Importance of Contrast , 2012, Neuron.

[36]  L. Koessler,et al.  Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia , 2012, Neuroscience.

[37]  A. Oliva,et al.  A Real-World Size Organization of Object Responses in Occipitotemporal Cortex , 2012, Neuron.

[38]  K. Grill-Spector,et al.  Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception , 2012, The Journal of Neuroscience.

[39]  Elias B. Issa,et al.  Precedence of the Eye Region in Neural Processing of Faces , 2012, The Journal of Neuroscience.

[40]  Bevil R. Conway,et al.  Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex , 2013, Nature Neuroscience.

[41]  Amy M. Ni,et al.  Insights into cortical mechanisms of behavior from microstimulation experiments , 2013, Progress in Neurobiology.

[42]  Roger B. H. Tootell,et al.  A curvature-processing network in macaque visual cortex , 2013 .

[43]  Leslie G. Ungerleider,et al.  Curvature-processing network in macaque visual cortex , 2014, Proceedings of the National Academy of Sciences.

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

[45]  D. Leopold,et al.  Face-selective neurons maintain consistent visual responses across months , 2014, Proceedings of the National Academy of Sciences.

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

[47]  Doris Y. Tsao,et al.  Intelligent Information Loss: The Coding of Facial Identity, Head Pose, and Non-Face Information in the Macaque Face Patch System , 2015, The Journal of Neuroscience.

[48]  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.

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