Dissociating the neural bases of repetition-priming and adaptation in the human brain for faces.

The repetition of a given stimulus leads to the attenuation of the functional magnetic resonance imaging (fMRI) signal compared with unrepeated stimuli, a phenomenon called fMRI adaptation or repetition suppression (RS). Previous studies have related RS of the fMRI signal behaviorally both to improved performance for the repeated stimulus (priming) and to shifts of perception away from the first stimulus (adaptation-related aftereffects). Here we used identical task (sex discrimination), trial structure [stimulus 1 (S1): 3,000 ms, interstimulus interval: 600 ms, stimulus 2 (S2): 300 ms], and S2 stimuli (androgynous faces) to test how RS of the face-specific areas of the occipito-temporal cortex relates to priming and aftereffects. By varying S1, we could induce priming (significantly faster reaction times when S1 and S2 were identical compared with different images) as well as sex-specific aftereffect [an increased ratio of male responses if S1 was a female face compared with ambiguous faces or to Fourier-randomized noise (FOU) images]. Presenting any face as S1 led to significant RS of the blood oxygen level-dependent signal in the fusiform and occipital face areas as well as in the lateral occipital cortex of both hemispheres compared with FOU, reflecting stimulus category-specific encoding. Additionally, while sex-specific adaptation effects were only observed in occipital face areas, primed trials led to a signal reduction in both face-selective regions. Altogether, these results suggest the differential neural mechanisms of adaptation and repetition priming.

[1]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[2]  S. Magnussen Low-level memory processes in vision , 2000, Trends in Neurosciences.

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

[4]  E. Cooper,et al.  The Priming of Face Recognition after Metric Transformations , 2002, Perception.

[5]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[6]  R. Goebel,et al.  Cerebral Cortex doi:10.1093/cercor/bhj005 Impaired Face Discrimination in Acquired Prosopagnosia Is Associated with Abnormal Response to Individual Faces in the Right Middle Fusiform Gyrus , 2005 .

[7]  Maneesh C. Patel,et al.  Distinct frontal systems for response inhibition, attentional capture, and error processing , 2010, Proceedings of the National Academy of Sciences.

[8]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[9]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[10]  S. Pollmann,et al.  Retinotopic Activation in Response to Subjective Contours in Primary Visual Cortex , 2008, Frontiers in human neuroscience.

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

[12]  F. Campbell,et al.  The tilt after-effect: a fresh look. , 1971, Vision research.

[13]  R. Vogels,et al.  Repetition Probability Does Not Affect fMRI Repetition Suppression for Objects , 2013, The Journal of Neuroscience.

[14]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Vogels,et al.  Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. , 2010, Cerebral cortex.

[16]  Bruno Rossion,et al.  Category Specificity in Early Perception: Face and Word N170 Responses Differ in Both Lateralization and Habituation Properties , 2008, Frontiers in human neuroscience.

[17]  A. Burton,et al.  N250r: a face-selective brain response to stimulus repetitions , 2004, Neuroreport.

[18]  Pawan Sinha,et al.  Imaging prior information in the brain , 2012, Proceedings of the National Academy of Sciences.

[19]  G. Orban,et al.  Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm , 2006, Neuron.

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

[21]  Gyula Kovács,et al.  Neural Correlates of Generic versus Gender-specific Face Adaptation , 2010, Journal of Cognitive Neuroscience.

[22]  Daniel Güllmar,et al.  Perceiving age and gender in unfamiliar faces: An fMRI study on face categorization , 2012, Brain and Cognition.

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

[24]  R. Henson,et al.  Priming, response learning and repetition suppression , 2008, Neuropsychologia.

[25]  D. Schacter,et al.  Cortical activity reductions during repetition priming can result from rapid response learning , 2004, Nature.

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

[27]  Mark W. Greenlee,et al.  Stimulus repetition probability effects on repetition suppression are position invariant for faces , 2012, NeuroImage.

[28]  G. Kovács,et al.  Position-specificity of facial adaptation , 2005, Neuroreport.

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

[30]  Reginald B. Adams,et al.  The neural basis of categorical face perception: graded representations of face gender in fusiform and orbitofrontal cortices. , 2010, Cerebral cortex.

[31]  K. D'ostilio,et al.  Dissociation between unconscious motor response facilitation and conflict in medial frontal areas , 2012, The European journal of neuroscience.

[32]  Ione Fine,et al.  The Relationship between Task Performance and Functional Magnetic Resonance Imaging Response , 2005, The Journal of Neuroscience.

[33]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[34]  D. Schacter,et al.  Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex , 2001, Neuropsychologia.

[35]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[36]  Alessandro Treves,et al.  How recent experience affects the perception of ambiguous objects , 2010, Brain Research.

[37]  Gilles Pourtois,et al.  Portraits or People? Distinct Representations of Face Identity in the Human Visual Cortex , 2005, Journal of Cognitive Neuroscience.

[38]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[39]  G. Kovács,et al.  Adaptation duration affects the spatial selectivity of facial aftereffects , 2007, Vision Research.

[40]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[41]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[42]  V. Goffaux,et al.  Spatio-temporal localization of the face inversion effect: an event-related potentials study , 1999, Biological Psychology.

[43]  Amanda Ellison,et al.  Event-related Repetitive TMS Reveals Distinct, Critical Roles for Right OFA and Bilateral Posterior STS in Judging the Sex and Trustworthiness of Faces , 2011, Journal of Cognitive Neuroscience.

[44]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[45]  Jody C. Culham,et al.  The relationship between fMRI adaptation and repetition priming , 2006, NeuroImage.

[46]  A. Burton,et al.  Event-related brain potential evidence for a response of inferior temporal cortex to familiar face repetitions. , 2002, Brain research. Cognitive brain research.

[47]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

[48]  David M. Grayson,et al.  You looking at me? , 1999, Nature.

[49]  R. Näsänen Spatial frequency bandwidth used in the recognition of facial images , 1999, Vision Research.

[50]  D. Burr,et al.  Visual aftereffects , 2009, Current Biology.

[51]  F. Keil,et al.  Categorical effects in the perception of faces , 1995, Cognition.

[52]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[53]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[54]  C. Jacques,et al.  The Speed of Individual Face Categorization , 2006, Psychological science.

[55]  K. Nakayama,et al.  Rapid face-selective adaptation of an early extrastriate component in MEG. , 2006, Cerebral cortex.

[56]  A. Young,et al.  Repetition priming of face recognition , 1987, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[57]  Yuhong Jiang,et al.  Inferior parietal lobule supports decision making under uncertainty in humans. , 2009, Cerebral cortex.

[58]  Bruno Rossion,et al.  Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170 , 2008, NeuroImage.

[59]  Two loci of repetition priming in the recognition of familiar faces. , 1996 .

[60]  Frans A. J. Verstraten,et al.  The motion aftereffect , 1998, Trends in Cognitive Sciences.

[61]  Luca Passamonti,et al.  Changes in “Top-Down” Connectivity Underlie Repetition Suppression in the Ventral Visual Pathway , 2011, The Journal of Neuroscience.

[62]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[63]  Jacqueline C. Snow,et al.  Gender-selective neural populations: evidence from event-related fMRI repetition suppression , 2013, Experimental Brain Research.

[64]  R. Sekuler,et al.  Aftereffect of Seen Motion with a Stabilized Retinal Image , 1963, Science.

[65]  Raymond J. Dolan,et al.  Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence , 2005, NeuroImage.

[66]  E. Gibson Linguistic complexity: locality of syntactic dependencies , 1998, Cognition.

[67]  K. Nakayama,et al.  Rapid adaptation of the m170 response: importance of face parts. , 2008, Cerebral cortex.

[68]  G. Deco,et al.  Neuronal Adaptation Effects in Decision Making , 2011, The Journal of Neuroscience.

[69]  B. Murphy,et al.  Adaptation to natural facial categories , 2022 .

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

[71]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[72]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[73]  A W Ellis,et al.  Two loci of repetition priming in the recognition of familiar faces. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[74]  R. Jenkins,et al.  Are you looking at me? Neural correlates of gaze adaptation , 2007, Neuroreport.

[75]  Otto H. MacLin,et al.  Figural aftereffects in the perception of faces , 1999, Psychonomic bulletin & review.

[76]  Jonas Larsson,et al.  fMRI repetition suppression: neuronal adaptation or stimulus expectation? , 2012, Cerebral cortex.

[77]  M. Eimer,et al.  The N170 component and its links to configural face processing: A rapid neural adaptation study , 2011, Brain Research.

[78]  Y. Goshen-Gottstein,et al.  Repetition priming for familiar and unfamiliar faces in a sex-judgment task: evidence for a common route for the processing of sex and identity. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[79]  Mark W. Greenlee,et al.  Position-specific and position-invariant face aftereffects reflect the adaptation of different cortical areas , 2008, NeuroImage.

[80]  Alex Martin,et al.  Long-lasting cortical plasticity in the object naming system , 2000, Nature Neuroscience.

[81]  Éva M. Bankó,et al.  Electrophysiological correlates of visual adaptation to faces and body parts in humans. , 2006, Cerebral cortex.

[82]  L. Deouell,et al.  Neural adaptation is related to face repetition irrespective of identity: a reappraisal of the N170 effect , 2011, Experimental Brain Research.

[83]  K. Nakayama,et al.  The effect of face inversion on the human fusiform face area , 1998, Cognition.

[84]  M. Bindemann,et al.  Brain potential correlates of face recognition: geometric distortions and the N250r brain response to stimulus repetitions. , 2008, Psychophysiology.

[85]  C. Clifford Perceptual adaptation: motion parallels orientation , 2002, Trends in Cognitive Sciences.

[86]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[87]  K. Grill-Spector,et al.  Object-selective cortex exhibits performance-independent repetition suppression. , 2006, Journal of neurophysiology.

[88]  Rufin Vogels,et al.  Stimulus repetition probability does not affect repetition suppression in macaque inferior temporal cortex. , 2011, Cerebral cortex.

[89]  H. Wilson,et al.  fMRI evidence for the neural representation of faces , 2005, Nature Neuroscience.

[90]  Werner Sommer,et al.  Repetition priming and associative priming of face recognition: Evidence from event-related potentials. , 1995 .

[91]  Irene E. Nagel,et al.  Human Aging Magnifies Genetic Effects on Executive Functioning and Working Memory , 2008, Frontiers in human neuroscience.

[92]  G. Kovács,et al.  Neural correlates of priming and adaptation in familiar face perception , 2013, Cortex.

[93]  G. Rhodes,et al.  Perceptual adaptation helps us identify faces , 2010, Vision Research.

[94]  G. Campana,et al.  Separate motion-detecting mechanisms for first- and second-order patterns revealed by rapid forms of visual motion priming and motion aftereffect. , 2009, Journal of vision.

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

[96]  J. Barton,et al.  Adaptation improves discrimination of face identity , 2011, Proceedings of the Royal Society B: Biological Sciences.

[97]  Rafael Malach,et al.  Targeting the functional properties of cortical neurons using fMR-adaptation , 2012, NeuroImage.

[98]  G. Kovács,et al.  Neural correlates of high-level adaptation-related aftereffects. , 2010, Journal of neurophysiology.

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

[100]  M. Webster,et al.  Visual adaptation: Neural, psychological and computational aspects , 2007, Vision Research.

[101]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[102]  Michael P. Milham,et al.  Distinct neural mechanisms of risk and ambiguity: A meta-analysis of decision-making , 2006, NeuroImage.

[103]  Frans A. J. Verstraten,et al.  Perceptual manifestations of fast neural plasticity: Motion priming, rapid motion aftereffect and perceptual sensitization , 2005, Vision Research.

[104]  Raymond J. Dolan,et al.  Face adaptation aftereffects reveal anterior medial temporal cortex role in high level category representation , 2007, NeuroImage.

[105]  M. Webster,et al.  Visual adaptation and face perception , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.