Emergent processes in cognitive-emotional interactions

Emotion and cognition have been viewed as largely separate entities in the brain. Within this framework, significant progress has been made in understanding specific aspects of behavior. Research in the past two decades, however, has started to paint a different picture of brain organization, one in which network interactions are key to understanding complex behaviors. From both basic and clinical perspectives, the characterization of cognitive-emotional interactions constitutes a fundamental issue in the investigation of the mind and brain. This review will highlight the interactive and integrative potential that exists in the brain to bring together the cognitive and emotional domains. First, anatomical evidence will be provided, focusing on structures such as hypothalamus, basal forebrain, amygdala, cingulate cortex, orbitofrontal cortex, and insula. Data on functional interactions will then be discussed, followed by a discussion of a dual competition framework, which describes cognitive-emotional interactions in terms of perceptual and cognitive competition mechanisms.

[1]  Leah Krubitzer,et al.  In Search of a Unifying Theory of Complex Brain Evolution , 2009, Annals of the New York Academy of Sciences.

[2]  Kyle R. Cave,et al.  From searching for features to searching for threat: Drawing the boundary between preattentive and attentive vision , 2006 .

[3]  Luiz Pessoa,et al.  Target visibility and visual awareness modulate amygdala responses to fearful faces. , 2006, Cerebral cortex.

[4]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[5]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[6]  H. Pashler The Psychology of Attention , 1997 .

[7]  Brent A. Vogt,et al.  Cingulate Neurobiology and Disease , 2009 .

[8]  Leticia de Oliveira,et al.  Attention and emotion , 2010, Scholarpedia.

[9]  Daniel G Bobrow,et al.  On data-limited and resource-limited processes , 1975, Cognitive Psychology.

[10]  D. Amaral,et al.  The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey , 2005, The Journal of comparative neurology.

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

[12]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[13]  Robert Ward,et al.  Response to Visual Threat Following Damage to the Pulvinar , 2005, Current Biology.

[14]  Leslie G. Ungerleider,et al.  Neuroimaging studies of attention and the processing of emotion-laden stimuli. , 2004, Progress in brain research.

[15]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[16]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[17]  L. Swanson,et al.  The structural organization of connections between hypothalamus and cerebral cortex 1 Published on the World Wide Web on 2 June 1997. 1 , 1997, Brain Research Reviews.

[18]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[19]  Rob Jenkins,et al.  Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. , 2007, Cerebral cortex.

[20]  L. Pessoa To what extent are emotional visual stimuli processed without attention and awareness? , 2005, Current Opinion in Neurobiology.

[21]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[22]  Luiz Pessoa,et al.  Affective Learning Enhances Visual Detection and Responses in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[23]  A. Anderson Affective influences on the attentional dynamics supporting awareness. , 2005, Journal of experimental psychology. General.

[24]  L. Pessoa,et al.  Embedding Reward Signals into Perception and Cognition , 2010, Front. Neurosci..

[25]  J. de Houwer,et al.  Do emotional stimuli interfere with response inhibition? Evidence from the stop signal paradigm , 2007 .

[26]  Luiz Pessoa,et al.  Segregating the significant from the mundane on a moment-to-moment basis via direct and indirect amygdala contributions , 2009, Proceedings of the National Academy of Sciences.

[27]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[28]  Joseph L. Price Architectonic structure of the orbital and medial prefrontal cortex , 2006 .

[29]  P. Holland,et al.  Amygdala circuitry in attentional and representational processes , 1999, Trends in Cognitive Sciences.

[30]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[31]  J. Eastwood,et al.  Perception without awareness: perspectives from cognitive psychology , 2001, Cognition.

[32]  Joseph E LeDoux The emotional brain , 1996 .

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

[34]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[35]  Changiz Geula,et al.  Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: A choline acetyltransferase study , 1992, The Journal of comparative neurology.

[36]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[37]  J. Duncan,et al.  Intelligence and the Frontal Lobe: The Organization of Goal-Directed Behavior , 1996, Cognitive Psychology.

[38]  M. Eysenck,et al.  Anxiety and cognitive performance: attentional control theory. , 2007, Emotion.

[39]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[40]  Z. Nadasdy,et al.  The Basal Forebrain Corticopetal System Revisited , 1999, Annals of the New York Academy of Sciences.

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

[42]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

[43]  Abnormal regulation of corticopetal cholinergic neurons and impaired information processing in neuropsychiatric disorders , 1999 .

[44]  Stan B. Floresco,et al.  Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making , 2008, Cognitive, affective & behavioral neuroscience.

[45]  D. Kahneman,et al.  Attention and Effort , 1973 .

[46]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[47]  David H. Zald,et al.  The Orbitofrontal Cortex , 2008 .

[48]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[49]  Robert Ward,et al.  Emotion recognition following human pulvinar damage , 2007, Neuropsychologia.

[50]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

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

[52]  Lisa Feldman Barrett,et al.  Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies , 2008, NeuroImage.

[53]  S. Shipp The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[54]  R. Dolan,et al.  Emotion, Cognition, and Behavior , 2002, Science.

[55]  S. Grossberg How does a brain build a cognitive code , 1980 .

[56]  H. Barbas,et al.  Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression , 2003, BMC Neuroscience.

[57]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[58]  R. Guimerà,et al.  Functional cartography of complex metabolic networks , 2005, Nature.

[59]  J. Eastwood,et al.  Differential attentional guidance by unattended faces expressing positive and negative emotion , 2001, Perception & psychophysics.

[60]  O. Sporns,et al.  Identification and Classification of Hubs in Brain Networks , 2007, PloS one.

[61]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[62]  H. Barbas,et al.  Topographic Organization of Connections between the Hypothalamus and Prefrontal Cortex in the Rhesus Monkey , 2022 .

[63]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[64]  Sonia J. Bishop,et al.  Neurocognitive mechanisms of anxiety: an integrative account , 2007, Trends in Cognitive Sciences.

[65]  L. Pessoa Emotion and cognition and the amygdala: From “what is it?” to “what's to be done?” , 2010, Neuropsychologia.

[66]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[67]  Malcolm P. Young,,et al.  Analysis of Connectivity: Neural Systems in the Cerebral Cortex , 1994, Reviews in the neurosciences.

[68]  L. Heimer,et al.  The limbic lobe and its output channels: Implications for emotional functions and adaptive behavior , 2006, Neuroscience & Biobehavioral Reviews.

[69]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[70]  L. Pessoa,et al.  Pulvinar and Affective Significance: Responses Track Moment-to-Moment Stimulus Visibility , 2010, Front. Hum. Neurosci..

[71]  Katya Rubia,et al.  Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection , 2003, NeuroImage.

[72]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[73]  Luiz Pessoa,et al.  Affective learning modulates spatial competition during low-load attentional conditions , 2008, Neuropsychologia.

[74]  E. Neafsey,et al.  Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. , 1990, Progress in brain research.

[75]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[76]  L. F. Barrett,et al.  Affect as a Psychological Primitive. , 2009, Advances in experimental social psychology.

[77]  Claus C. Hilgetag,et al.  Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala , 2007, NeuroImage.

[78]  L. Swanson Cerebral hemisphere regulation of motivated behavior 1 1 Published on the World Wide Web on 2 November 2000. , 2000, Brain Research.

[79]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

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

[81]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[82]  E. Lauterbach The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1993 .

[83]  John G. Taylor,et al.  Influence of attentional demands on the processing of emotional facial expressions in the amygdala , 2007, NeuroImage.

[84]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[85]  J. Aggleton,et al.  Primate evolution and the amygdala , 2000 .

[86]  L. Swanson,et al.  What is the amygdala? , 1998, Trends in Neurosciences.

[87]  A. Nuñez,et al.  Electrophysiological evidence for the existence of a posterior cortical–prefrontal–basal forebrain circuitry in modulating sensory responses in visual and somatosensory rat cortical areas , 2003, Neuroscience.

[88]  Yihong Yang,et al.  Neural substrates of the interaction of emotional stimulus processing and motor inhibitory control: An emotional linguistic go/no-go fMRI study , 2007, NeuroImage.

[89]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[90]  P. Holland,et al.  Lesions of the Amygdala Central Nucleus Alter Performance on a Selective Attention Task , 2000, The Journal of Neuroscience.

[91]  P. Lang,et al.  Fear and anxiety: animal models and human cognitive psychophysiology. , 2000, Journal of affective disorders.

[92]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[93]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[94]  Michael J. Goard,et al.  Basal Forebrain Activation Enhances Cortical Coding of Natural Scenes , 2009, Nature Neuroscience.

[95]  G. Fricchione Descartes’ Error: Emotion, Reason and the Human Brain , 1995 .

[96]  S. Wiens Subliminal emotion perception in brain imaging: findings, issues, and recommendations. , 2006, Progress in brain research.

[97]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[98]  P. Holland,et al.  Different Roles for Amygdala Central Nucleus and Substantia Innominata in the Surprise-Induced Enhancement of Learning , 2006, The Journal of Neuroscience.

[99]  M. Carrasco,et al.  PSYCHOLOGICAL SCIENCE Research Article Emotion Facilitates Perception and Potentiates the Perceptual Benefits of Attention , 2022 .

[100]  M. Sarter,et al.  Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents , 1999, Neuroscience.

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

[102]  D. S. Zahm,et al.  The evolving theory of basal forebrain functional—anatomical ‘macrosystems’ , 2006, Neuroscience & Biobehavioral Reviews.

[103]  John Duncan,et al.  State Anxiety Modulation of the Amygdala Response to Unattended Threat-Related Stimuli , 2004, The Journal of Neuroscience.

[104]  L. F. Barrett,et al.  Affect is a form of cognition: A neurobiological analysis , 2007, Cognition & emotion.

[105]  L. Pessoa,et al.  Neural Correlates of Perceptual Choice and Decision Making during Fear–Disgust Discrimination , 2007, The Journal of Neuroscience.

[106]  A. Mathews,et al.  A Cognitive Model of Selective Processing in Anxiety , 1998, Cognitive Therapy and Research.

[107]  L. Pessoa,et al.  Dissociable effects of bottom-up and top-down factors on the processing of unattended fearful faces , 2007, Neuropsychologia.

[108]  J. Bullier,et al.  Response modulations by static texture surround in area V1 of the macaque monkey do not depend on feedback connections from V2. , 2001, Journal of neurophysiology.

[109]  L. Swanson The Amygdala and Its Place in the Cerebral Hemisphere , 2003, Annals of the New York Academy of Sciences.

[110]  Patrik Vuilleumier,et al.  Emotional facial expressions capture attention , 2001, Neurology.

[111]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

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

[113]  M. Raichle,et al.  Integration of emotion and cognition in the lateral prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[114]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[115]  Naotsugu Tsuchiya,et al.  Intact rapid detection of fearful faces in the absence of the amygdala , 2009, Nature Neuroscience.

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

[117]  J. Bullier,et al.  Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. , 1989, Journal of neurophysiology.

[118]  Thomas Elbert,et al.  Dissociation in human prefrontal cortex of affective influences on working memory-related activity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[119]  D. Amaral,et al.  Synaptic organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey , 2005, The Journal of comparative neurology.

[120]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[121]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[122]  Marc D. Lewis Bridging emotion theory and neurobiology through dynamic systems modeling , 2005, Behavioral and Brain Sciences.

[123]  Jon H Kaas,et al.  Evolution of somatosensory and motor cortex in primates. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[124]  H. Barbas,et al.  Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex , 1995, Neuroscience & Biobehavioral Reviews.

[125]  Tor D. Wager,et al.  Cognitive and Motivational Functions of the Human Prefrontal Cortex , 2009 .

[126]  Jillian H. Fecteau,et al.  Salience, relevance, and firing: a priority map for target selection , 2006, Trends in Cognitive Sciences.

[127]  D. Norman,et al.  Attention to action: Willed and automatic control , 1980 .

[128]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.