Reprint of: Emotion and cognition and the amygdala: From “what is it?” to “what's to be done?”

The amygdala is a fascinating, complex structure that lies at the center of much of our current thinking about emotion. Here, I will review data that suggest that the amygdala is involved in several processes linked to determining what a stimulus is and what the organism should therefore do - the two questions that are part of the title. This piece will focus on three main aspects of amygdala function, namely attention, value representation, and decision making, by reviewing both non-human and human data. Two mechanisms of affective attention will be described. The first involves projections from the central nucleus of the amygdala to the basal forebrain, which has extensive and diffuse projections throughout the cortical mantle. The second involves projections from the basal amygdala to multiple levels across the visual cortex. I will also describe how the basolateral amygdala is important for the representation of value and in decision making. Overall, it will be argued that the amygdala plays a key role in solving the following problem: How can a limited-capacity information processing system that receives a constant stream of diverse inputs be designed to selectively process those inputs that are most significant to the objectives of the system? "What is it?" and "What's to be done?" processes can then be viewed as important building blocks in the construction of emotion, a process that is intertwined with cognition. Furthermore, answering the two questions directs how resources should be mobilized as the organism seeks out additional information from the environment.

[1]  E. Phelps,et al.  The human amygdala. , 2009 .

[2]  P. Holland,et al.  Effects of amygdala central nucleus lesions on blocking and unblocking. , 1993, Behavioral neuroscience.

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

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

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

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

[7]  D. S. Zahm,et al.  Anatomy of Neuropsychiatry: The New Anatomy of the Basal Forebrain and Its Implications for Neuropsychiatric Illness , 2007 .

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

[9]  H. Ursin,et al.  Functional localization within the amygdaloid complex in the cat. , 1960, Electroencephalography and clinical neurophysiology.

[10]  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.

[11]  K. Pribram,et al.  Arousal, activation, and effort in the control of attention. , 1975, Psychological review.

[12]  M. Sarter,et al.  Basal Forebrain Afferent Projections Modulating Cortical Acetylcholine, Attention, and Implications for Neuropsychiatric Disorders , 1999, Annals of the New York Academy of Sciences.

[13]  B. Kaada Stimulation and Regional Ablation of the Amygdaloid Complex with Reference to Functional Representations , 1972 .

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

[15]  M. Sarter,et al.  Abnormal regulation of corticopetal cholinergic neurons and impaired information processing in neuropsychiatric disorders , 1999, Trends in Neurosciences.

[16]  Christian Büchel,et al.  Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans , 2010, Proceedings of the National Academy of Sciences.

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

[18]  J. Germana Central efferent processes and autonomic-behavioral integration. , 1969, Psychophysiology.

[19]  B. Kapp,et al.  Effects of electrical stimulation of the amygdaloid central nucleus on neocortical arousal in the rabbit. , 1994, Behavioral neuroscience.

[20]  A. Tversky,et al.  Prospect theory: analysis of decision under risk , 1979 .

[21]  M. Sarter,et al.  Article Prefrontal Acetylcholine Release Controls Cue Detection on Multiple Timescales , 2022 .

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

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

[24]  D. Kumaran,et al.  Frames, Biases, and Rational Decision-Making in the Human Brain , 2006, Science.

[25]  Fabian Grabenhorst,et al.  Role of the amygdala in decisions under ambiguity and decisions under risk: Evidence from patients with Urbach-Wiethe disease , 2007, Neuropsychologia.

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

[28]  S. Grossberg,et al.  Neural dynamics of attentionally modulated Pavlovian conditioning: blocking, interstimulus interval, and secondary reinforcement. , 1987, Applied optics.

[29]  Sara E. Morrison,et al.  Re-valuing the amygdala , 2010, Current Opinion in Neurobiology.

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

[31]  Guillem R. Esber,et al.  All that glitters ... dissociating attention and outcome expectancy from prediction errors signals. , 2010, Journal of neurophysiology.

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

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

[34]  Richard S. Sutton,et al.  Reinforcement Learning , 1992, Handbook of Machine Learning.

[35]  T. Robbins,et al.  Neurobehavioural mechanisms of reward and motivation , 1996, Current Opinion in Neurobiology.

[36]  T. Robbins,et al.  Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice , 2004, The Journal of Neuroscience.

[37]  Marvin M. Chun,et al.  Attentional modulation of the amygdala varies with personality , 2006, NeuroImage.

[38]  E. Murray The amygdala, reward and emotion , 2007, Trends in Cognitive Sciences.

[39]  Geoffrey Schoenbaum,et al.  Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task , 2003, The Journal of Neuroscience.

[40]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[41]  J. Aggleton,et al.  The amygdala - what's happened in the last decade? , 2000 .

[42]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[43]  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.

[44]  Marvin M. Chun,et al.  Attentional rubbernecking: Cognitive control and personality in emotion-induced blindness , 2005, Psychonomic bulletin & review.

[45]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[46]  J. Pearce,et al.  A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980 .

[47]  C. Koch,et al.  Imagery neurons in the human brain , 2000, Nature.

[48]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.

[49]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[50]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[51]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[52]  Stefano Fusi,et al.  Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. , 2010, Annual review of neuroscience.

[53]  C. Koch,et al.  Latency and Selectivity of Single Neurons Indicate Hierarchical Processing in the Human Medial Temporal Lobe , 2008, The Journal of Neuroscience.

[54]  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.

[55]  Katrin Amunts,et al.  Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain , 2008, NeuroImage.

[56]  Gregory P. Lee,et al.  Different Contributions of the Human Amygdala and Ventromedial Prefrontal Cortex to Decision-Making , 1999, The Journal of Neuroscience.

[57]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[58]  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.

[59]  T. Robbins,et al.  Central cholinergic systems and cognition. , 1997, Annual review of psychology.

[60]  A. Tversky,et al.  Prospect Theory : An Analysis of Decision under Risk Author ( s ) : , 2007 .

[61]  R. Dolan,et al.  Automatic relevance detection in the absence of a functional amygdala , 2011, Neuropsychologia.

[62]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

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

[64]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[65]  G. Stock,et al.  Cardiovascular changes during arousal elicited by stimulation of amygdala, hypothalamus and locus coeruleus. , 1981, Journal of the autonomic nervous system.

[66]  M. Roesch,et al.  Cocaine-induced decision-making deficits are mediated by miscoding in basolateral amygdala , 2007, Nature Neuroscience.

[67]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[68]  Angela D. Friederici,et al.  Diffusion tensor imaging segments the human amygdala in vivo , 2010, NeuroImage.

[69]  Stephen D. Smith,et al.  The naked truth: Positive, arousing distractors impair rapid target perception , 2007 .

[70]  S. Floresco,et al.  Amygdala-prefrontal cortical circuitry regulates effort-based decision making. , 2006, Cerebral cortex.

[71]  Kaada Br,et al.  Somato-motor, autonomic and electrocorticographic responses to electrical stimulation of rhinencephalic and other structures in primates, cat, and dog; a study of responses from the limbic, subcallosal, orbito-insular, piriform and temporal cortex, hippocampus-fornix and amygdala. , 1951 .

[72]  Joseph J. Paton,et al.  Expectation Modulates Neural Responses to Pleasant and Aversive Stimuli in Primate Amygdala , 2007, Neuron.

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

[74]  Guillem R. Esber,et al.  Neural Correlates of Variations in Event Processing during Learning in Basolateral Amygdala , 2010, The Journal of Neuroscience.

[75]  Stephen D. Smith,et al.  Fear-enhanced visual search persists after amygdala lesions , 2010, Neuropsychologia.

[76]  K M Gothard,et al.  Neural responses to facial expression and face identity in the monkey amygdala. , 2007, Journal of neurophysiology.

[77]  A. Bechara,et al.  PSYCHOLOGICAL SCIENCE Research Article Neural Correlates of Adaptive Decision Making for Risky Gains and Losses , 2022 .

[78]  S. Floresco,et al.  Fundamental Contribution by the Basolateral Amygdala to Different Forms of Decision Making , 2009, The Journal of Neuroscience.

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

[80]  A. Lüthi,et al.  Processing of Temporal Unpredictability in Human and Animal Amygdala , 2007, The Journal of Neuroscience.

[81]  J. O'Doherty,et al.  Contributions of the Amygdala to Reward Expectancy and Choice Signals in Human Prefrontal Cortex , 2007, Neuron.

[82]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

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

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

[85]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[86]  T. Robbins,et al.  Amygdala-ventral striatal interactions and reward-related processes. , 1992 .

[87]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[88]  J. O'Doherty,et al.  Regret and its avoidance: a neuroimaging study of choice behavior , 2005, Nature Neuroscience.

[89]  Olavi Eränkö,et al.  Histochemical Evidence of Intense Phosphatase Activity in the Hypothalamic Magnocellular Nuclei of the Rat , 1951 .

[90]  R. Dolan,et al.  Emotion, Decision Making, and the Amygdala , 2008, Neuron.

[91]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[92]  M. Sarter,et al.  Cholinergic Mediation of Attention , 2008, Annals of the New York Academy of Sciences.

[93]  B. Richmond,et al.  Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules , 2005, The Journal of Neuroscience.

[94]  B T Hyman,et al.  Neuropsychological correlates of bilateral amygdala damage. , 1990, Archives of neurology.

[95]  L. Swanson,et al.  Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems , 2001, Brain Research Reviews.

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

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

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

[99]  Ben Seymour,et al.  Neural Activity Associated with the Passive Prediction of Ambiguity and Risk for Aversive Events , 2009, The Journal of Neuroscience.

[100]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[101]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

[102]  M. Nicolelis,et al.  Neuronal Ensemble Bursting in the Basal Forebrain Encodes Salience Irrespective of Valence , 2008, Neuron.

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

[104]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

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

[106]  Joseph J. Paton,et al.  Moment-to-Moment Tracking of State Value in the Amygdala , 2008, The Journal of Neuroscience.

[107]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.