Multiple synergistic effects of emotion and memory on proactive processes leading to scene recognition

Visual scene recognition is a proactive process through which contextual cues and top-down expectations facilitate the extraction of invariant features. Whether the emotional content of the scenes exerts a reliable influence on these processes or not, however, remains an open question. Here, topographic ERP mapping analysis and a distributed source localization method were used to characterize the electrophysiological correlates of proactive processes leading to scene recognition, as well as the potential modulation of these processes by memory and emotion. On each trial, the content of a complex neutral or emotional scene was progressively revealed, and participants were asked to decide whether this scene had previously been encountered or not (delayed match-to-sample task). Behavioral results showed earlier recognition for old compared to new scenes, as well as delayed recognition for emotional vs. neutral scenes. Electrophysiological results revealed that, ~400 ms following stimulus onset, activity in ventral object-selective regions increased linearly as a function of accumulation of perceptual evidence prior to recognition of old scenes. The emotional content of the scenes had an early influence in these areas. By comparison, at the same latency, the processing of new scenes was mostly achieved by dorsal and medial frontal brain areas, including the anterior cingulate cortex and the insula. In the latter region, emotion biased recognition at later stages, likely corresponding to decision making processes. These findings suggest that emotion can operate at distinct and multiple levels during proactive processes leading to scene recognition, depending on the extent of prior encounter with these scenes.

[1]  John C. Mazziotta,et al.  A Probabilistic Atlas and Reference System for the Human Brain , 2001 .

[2]  Michael D. Rugg,et al.  Recognition memory with and without retrieval of context: An event-related potential study , 1995, Neuropsychologia.

[3]  B. Mesquita,et al.  Context in Emotion Perception , 2011 .

[4]  Goldman-Rakic Ps Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. , 1990 .

[5]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[6]  Jennifer L. Ferris,et al.  Lateral inferior prefrontal cortex and anterior cingulate cortex are engaged at different stages in the solution of insight problems , 2009, Proceedings of the National Academy of Sciences.

[7]  Kirsten G. Volz,et al.  A common neural system signaling the need for behavioral changes , 2004, Trends in Cognitive Sciences.

[8]  Ken A. Paller,et al.  Neural Manifestations of Memory with and without Awareness , 2003, Neuron.

[9]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[10]  Ken A. Paller,et al.  Brain substrates of implicit and explicit memory: The importance of concurrently acquired neural signals of both memory types , 2008, Neuropsychologia.

[11]  P. Sajda,et al.  EEG-Informed fMRI Reveals Spatiotemporal Characteristics of Perceptual Decision Making , 2007, The Journal of Neuroscience.

[12]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[13]  C. Summerfield,et al.  Expectation (and attention) in visual cognition , 2009, Trends in Cognitive Sciences.

[14]  S. Delplanque,et al.  Beyond Conventional Event-related Brain Potential (ERP): Exploring the Time-course of Visual Emotion Processing Using Topographic and Principal Component Analyses , 2008, Brain Topography.

[15]  Beatrice de Gelder,et al.  Context influences early perceptual analysis of faces--an electrophysiological study. , 2006, Cerebral cortex.

[16]  Joel L. Voss,et al.  Fluent Conceptual Processing and Explicit Memory for Faces Are Electrophysiologically Distinct , 2006, The Journal of Neuroscience.

[17]  M Esslen,et al.  Brain areas and time course of emotional processing , 2004, NeuroImage.

[18]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  Mark V. Albert,et al.  Anticipation of conflict monitoring in the anterior cingulate cortex and the prefrontal cortex , 2007, Proceedings of the National Academy of Sciences.

[20]  A. Hamm,et al.  Enhanced long-term recollection for emotional pictures: evidence from high-density ERPs. , 2009, Psychophysiology.

[21]  Adam K. Anderson,et al.  Affect-biased attention as emotion regulation , 2012, Trends in Cognitive Sciences.

[22]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[23]  S. Kotz,et al.  Emotion speeds up conflict resolution: a new role for the ventral anterior cingulate cortex? , 2011, Cerebral cortex.

[24]  D. Grandjean,et al.  Electrophysiological correlates of rapid spatial orienting towards fearful faces. , 2004, Cerebral cortex.

[25]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[26]  Christoph M. Michel,et al.  Towards the utilization of EEG as a brain imaging tool , 2012, NeuroImage.

[27]  Michael D. Rugg,et al.  Dissociation of the neural correlates of implicit and explicit memory , 1998, Nature.

[28]  M. Bar,et al.  Early onset of neural synchronization in the contextual associations network , 2011, Proceedings of the National Academy of Sciences.

[29]  M. Bar Visual objects in context , 2004, Nature Reviews Neuroscience.

[30]  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.

[31]  Dirk Hermans,et al.  Affective priming of nonaffective semantic categorization responses. , 2007, Experimental psychology.

[32]  B. de Gelder,et al.  Rapid influence of emotional scenes on encoding of facial expressions: an ERP study. , 2008, Social cognitive and affective neuroscience.

[33]  Catherine J. Norris,et al.  The current status of research on the structure of evaluative space , 2010, Biological Psychology.

[34]  Antonio Schettino,et al.  Brain dynamics of upstream perceptual processes leading to visual object recognition: A high density ERP topographic mapping study , 2011, NeuroImage.

[35]  Jan R. Wiersema,et al.  Cascade of Neural Events Leading from Error Commission to Subsequent Awareness Revealed Using EEG Source Imaging , 2011, PloS one.

[36]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[37]  M. Junghöfer,et al.  The selective processing of briefly presented affective pictures: an ERP analysis. , 2004, Psychophysiology.

[38]  J. Cacioppo,et al.  The affect system has parallel and integrative processing components: Form follows function. , 1999 .

[39]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[40]  R. Cabeza,et al.  Event-related potentials of emotional memory: Encoding pleasant, unpleasant, and neutral pictures , 2002, Cognitive, affective & behavioral neuroscience.

[41]  S. Kotz,et al.  Emotion triggers executive attention: Anterior cingulate cortex and amygdala responses to emotional words in a conflict task , 2011, Human brain mapping.

[42]  L. F. Barrett,et al.  Context Is Routinely Encoded During Emotion Perception , 2010, Psychological science.

[43]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[44]  D. Yarnitsky,et al.  Neurophysiology of the cortical pain network: revisiting the role of S1 in subjective pain perception via standardized low-resolution brain electromagnetic tomography (sLORETA). , 2008, Journal of Pain.

[45]  Moshe Bar,et al.  The proactive brain: memory for predictions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  Georg Engel,et al.  Propranolol selectively blocks the enhanced parietal old/new effect during long-term recollection of unpleasant pictures: A high density ERP study , 2010, NeuroImage.

[47]  Sabine Kastner,et al.  Interactive report A control of the processing of neutral and emotional stimuli , 2002 .

[48]  Christoph M. Michel,et al.  Spatiotemporal Dynamics of Human Cognition. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[49]  R. Cabeza,et al.  Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[51]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[52]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[53]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[54]  E. Halgren,et al.  Cognitive response profile of the human fusiform face area as determined by MEG. , 2000, Cerebral cortex.

[55]  J. Rohrbaugh,et al.  Electrocortical signs of levels of processing: perceptual analysis and recognition memory. , 1980, Psychophysiology.

[56]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[57]  T. Curran,et al.  Using ERPs to dissociate recollection from familiarity in picture recognition. , 2003, Brain research. Cognitive brain research.

[58]  J. de Houwer,et al.  On the (un)conditionality of automatic attitude activation: the valence proportion effect. , 2011, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[59]  H. Meeren,et al.  Beyond the face: exploring rapid influences of context on face processing. , 2006, Progress in brain research.

[60]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[61]  M. Junghöfer,et al.  Emotion and attention: event-related brain potential studies. , 2006, Progress in brain research.

[62]  A. Kleinschmidt,et al.  Anterior insula activations in perceptual paradigms: often observed but barely understood , 2010, Brain Structure and Function.

[63]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

[64]  B. Mesquita,et al.  The experience of emotion. , 2007, Annual review of psychology.

[65]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. II. Demonstration of Sublobar Accuracy in Patients with Simultaneous Surface and Depth Recordings , 2004, Brain Topography.

[66]  Joshua J. Tremel,et al.  High quality but limited quantity perceptual evidence produces neural accumulation in frontal and parietal cortex. , 2011, Cerebral cortex.

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

[68]  A. Treisman,et al.  Perceiving visually presented objets: recognition, awareness, and modularity , 1998, Current Opinion in Neurobiology.

[69]  Kensuke Sekihara,et al.  Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction , 2005, NeuroImage.

[70]  J. Russell A circumplex model of affect. , 1980 .

[71]  Peter Lang,et al.  Brain processes in emotional perception: Motivated attention , 2004 .

[72]  Antonio Schettino,et al.  Valence-Specific Modulation in the Accumulation of Perceptual Evidence Prior to Visual Scene Recognition , 2012, PloS one.

[73]  Michael D. Rugg,et al.  Further Dissociating the Processes Involved in Recognition Memory: An fMRI Study , 2005, Journal of Cognitive Neuroscience.

[74]  Robert Tibshirani,et al.  Cluster Validation by Prediction Strength , 2005 .

[75]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

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

[77]  Alice Mado Proverbio,et al.  Sex differences in the brain response to affective scenes with or without humans , 2009, Neuropsychologia.

[78]  M. Fuchs,et al.  A standardized boundary element method volume conductor model , 2002, Clinical Neurophysiology.

[79]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[80]  Frans A. J. Verstraten,et al.  Dynamics of visual recognition revealed by fMRI , 2006, NeuroImage.

[81]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

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

[83]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[84]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[85]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[86]  BrunetDenis,et al.  Spatiotemporal analysis of multichannel EEG , 2011 .

[87]  Claudio Pollo,et al.  Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients , 2011, Brain : a journal of neurology.

[88]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[89]  P. Lang The emotion probe. Studies of motivation and attention. , 1995, The American psychologist.

[90]  John Polich,et al.  Affective recognition memory processing and event-related brain potentials , 2011, Cognitive, affective & behavioral neuroscience.

[91]  A. Torralba,et al.  The role of context in object recognition , 2007, Trends in Cognitive Sciences.

[92]  Moshe Bar,et al.  See it with feeling: affective predictions during object perception , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[93]  J. Hegdé Time course of visual perception: Coarse-to-fine processing and beyond , 2008, Progress in Neurobiology.

[94]  H. Seo,et al.  Temporal Filtering of Reward Signals in the Dorsal Anterior Cingulate Cortex during a Mixed-Strategy Game , 2007, The Journal of Neuroscience.

[95]  M. Bar,et al.  Scenes Unseen: The Parahippocampal Cortex Intrinsically Subserves Contextual Associations, Not Scenes or Places Per Se , 2008, The Journal of Neuroscience.

[96]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[97]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[98]  L. Pessoa On the relationship between emotion and cognition , 2008, Nature Reviews Neuroscience.

[99]  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.

[100]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

[101]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[102]  Steven E. Petersen,et al.  Dissociating Early and Late Error Signals in Perceptual Recognition , 2008, Journal of Cognitive Neuroscience.

[103]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[104]  J. Cacioppo,et al.  Beyond Bipolar Conceptualizations and Measures: The Case of Attitudes and Evaluative Space , 1997, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[105]  R. Righart,et al.  Recognition of facial expressions is influenced by emotional scene gist , 2008, Cognitive, affective & behavioral neuroscience.

[106]  Gilles Pourtois,et al.  Modulation of Face Processing by Emotional Expression and Gaze Direction during Intracranial Recordings in Right Fusiform Cortex , 2010, Journal of Cognitive Neuroscience.

[107]  J. Uleman Consciousness and Control , 1987 .

[108]  D. Lehmann,et al.  Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. , 2002, Methods and findings in experimental and clinical pharmacology.

[109]  Eswar Damaraju,et al.  Affective learning enhances activity and functional connectivity in early visual cortex , 2009, Neuropsychologia.

[110]  Dietrich Lehmann,et al.  Mapping event-related brain potential microstates to sentence endings , 2005, Brain Topography.

[111]  Ulrich Mayr,et al.  Conflict, consciousness, and control , 2004, Trends in Cognitive Sciences.

[112]  Tim Curran,et al.  Picture Superiority Doubly Dissociates the ERP Correlates of Recollection and Familiarity , 2011, Journal of Cognitive Neuroscience.

[113]  A. Hamm,et al.  Emotional memories are resilient to time: Evidence from the parietal ERP old/new effect , 2011, Human brain mapping.

[114]  Markus Junghöfer,et al.  Selective Visual Attention to Emotion , 2007, The Journal of Neuroscience.

[115]  M. Rugg,et al.  An event-related potential study of recognition memory with and without retrieval of source. , 1996, Brain : a journal of neurology.

[116]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[117]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

[118]  S. Morand,et al.  Electric source imaging of human brain functions , 2001, Brain Research Reviews.

[119]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[120]  Chrysa D. Lithari,et al.  Are Females More Responsive to Emotional Stimuli? A Neurophysiological Study Across Arousal and Valence Dimensions , 2009, Brain Topography.

[121]  K. Scherer,et al.  Spatial frequencies or emotional effects? A systematic measure of spatial frequencies for IAPS pictures by a discrete wavelet analysis , 2007, Journal of Neuroscience Methods.

[122]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[123]  Valer Jurcak,et al.  10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems , 2007, NeuroImage.