Effects of long-term object familiarity on event-related potentials in the monkey.

Although some change in the neural representation of an object must occur as it becomes familiar, the nature of this change is not fully understood. In humans, it has been shown that the N170-an evoked visual potential-is enhanced for classes of objects for which people have visual expertise. In this study, we explored whether monkeys show a similar modulation in event-related potential (ERP) amplitude as a result of long-term familiarity by recording ERPs with chronically implanted electrodes over extended training periods spanning many sessions. In each of 3 experiments, we found larger amplitude visual evoked responses to highly familiar images for the time period of 120-250 ms after stimulus onset. This difference was found when the monkeys were trained in an individual-level discrimination task, in a task that required only color discrimination, and even following a viewing-only task. We thus observed this familiarity effect across several tasks and different object categories and further found that the difference between "familiar" and "novel" became smaller as the animals gained experience with the previously unfamiliar objects across multiple test sessions. These data suggest that changes in visual responses associated with familiarity are evident early in the evoked visual response, are robust, and may be automatic, driven at least in part by repeated object exposure.

[1]  Edward A. Wasserman,et al.  Conceptual Behavior in Pigeons : Categorization of Both Familiar and Novel Examples From Four Classes of Natural and Artificial Stimuli , 2009 .

[2]  E. Miller,et al.  Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. , 2005, Cerebral cortex.

[3]  I. Gauthier,et al.  A Perceptual Traffic Jam on Highway N170 , 2005 .

[4]  M. Tarr,et al.  Visual expertise with nonface objects leads to competition with the early perceptual processing of faces in the human occipitotemporal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Emerman,et al.  Ancient Adaptive Evolution of the Primate Antiviral DNA-Editing Enzyme APOBEC3G , 2004, PLoS biology.

[6]  Margot J. Taylor,et al.  Source analysis of the N170 to faces and objects , 2004, Neuroreport.

[7]  N. Sigala,et al.  Visual categorization and the inferior temporal cortex , 2004, Behavioural Brain Research.

[8]  N. Logothetis,et al.  The Effect of Learning on the Function of Monkey Extrastriate Visual Cortex , 2004, PLoS biology.

[9]  D. Jeffreys,et al.  Evoked potential evidence for human brain mechanisms that respond to single, fixated faces , 2004, Experimental Brain Research.

[10]  M. W. Brown,et al.  Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex , 2004, Experimental Brain Research.

[11]  Christian Hölscher,et al.  Perirhinal cortex neuronal activity related to long‐term familiarity memory in the macaque , 2003, The European journal of neuroscience.

[12]  R. Reid,et al.  Efficacy of Retinal Spikes in Driving Cortical Responses , 2003, The Journal of Neuroscience.

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

[14]  I. Gauthier,et al.  Perceptual interference supports a non-modular account of face processing , 2003, Nature Neuroscience.

[15]  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.

[16]  M. Behrmann,et al.  Impact of learning on representation of parts and wholes in monkey inferotemporal cortex , 2002, Nature Neuroscience.

[17]  I. Gauthier,et al.  A defense of the subordinate-level expertise account for the N170 component , 2002, Cognition.

[18]  M. Tarr,et al.  Expertise Training with Novel Objects Leads to Left-Lateralized Facelike Electrophysiological Responses , 2002, Psychological science.

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

[20]  S. Bentin,et al.  Domain specificity versus expertise: factors influencing distinct processing of faces , 2002, Cognition.

[21]  N. Sigala,et al.  Visual categorization shapes feature selectivity in the primate temporal cortex , 2002, Nature.

[22]  Florence Thibaut,et al.  ERPs ASSOCIATED WITH FAMILIARITY AND DEGREE OF FAMILIARITY DURING FACE RECOGNITION , 2002, The International journal of neuroscience.

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

[24]  Stephane A. Roy,et al.  Coincidence Detection or Temporal Integration? What the Neurons in Somatosensory Cortex Are Doing , 2001, The Journal of Neuroscience.

[25]  J. Tanaka,et al.  A Neural Basis for Expert Object Recognition , 2001, Psychological science.

[26]  Ravi S. Menon,et al.  The effects of visual object priming on brain activation before and after recognition , 2000, Current Biology.

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

[28]  L. Deouell,et al.  Cognitive Neuroscience: Selective visual streaming in face recognition: evidence from developmental prosopagnosia , 1999 .

[29]  R A McCarthy,et al.  Prosopagnosia and structural encoding of faces: evidence from event-related potentials. , 1999, Neuroreport.

[30]  E. Rolls,et al.  View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. , 1998, Cerebral cortex.

[31]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

[32]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

[33]  R L Buckner,et al.  Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[35]  Michael C. Doyle,et al.  Modulation of event-related potentials by the repetition of drawings of novel objects. , 1995, Brain research. Cognitive brain research.

[36]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[37]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

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

[39]  Andrew W. Ellis,et al.  ROLES OF WORD FREQUENCY AND AGE OF ACQUISITION IN WORD NAMING AND LEXICAL DECISION , 1995 .

[40]  G. Sebestyen,et al.  Face recognition as a function of social attention in non-human primates: an ERP study. , 1994, Brain research. Cognitive brain research.

[41]  Pierre Comon,et al.  Independent component analysis, A new concept? , 1994, Signal Process..

[42]  M. Mesulam,et al.  Differential neural activity in the human temporal lobe evoked by faces of family members and friends , 1993, Annals of neurology.

[43]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[44]  J. Pineda,et al.  Event-related potentials in macaque monkey during passive and attentional processing of faces in a priming paradigm , 1993, Behavioural Brain Research.

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

[46]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  E. Wasserman,et al.  Conceptual behavior in pigeons: Categories, subcategories, and pseudocategories. , 1988 .

[48]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.