Functional organization of the human amygdala in appetitive learning.

The amygdala is a small subcortical structure located bilaterally in medial temporal lobes. It is a key region for emotional processes and some forms of associative learning. In particular, the role of the amygdala in processing of negative emotions and aversive learning has been shown in numerous studies. However, involvement of this structure in processing of positive affect and appetitive learning is not fully understood. Previous experiments in animals are not consistent. While some authors implicate only the centromedial part of the amygdala in appetitive learning, the others suggest contribution of both centromedial and basolateral subregions. Although from the evolutionary perspective appetitive learning is equally important as aversive learning, research on the role of the human amygdala and its subregions in appetitive learning is undertaken relatively rarely and the results are not conclusive. Therefore, the aim of this review is twofold: to summarize the current knowledge in this field and to indicate and discuss the factors, which might affect the observed level of the amygdala activity during appetitive learning in humans.

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

[2]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[3]  Wolfgang M Pauli,et al.  In vivo delineation of subdivisions of the human amygdaloid complex in a high‐resolution group template , 2016, Human brain mapping.

[4]  Vivian V. Valentin,et al.  Determining the Neural Substrates of Goal-Directed Learning in the Human Brain , 2007, The Journal of Neuroscience.

[5]  Dan J Stein,et al.  The role of the basolateral amygdala in the perception of faces in natural contexts , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[6]  Thomas E. Nichols,et al.  Fixing the stimulus-as-fixed-effect fallacy in task fMRI , 2016, bioRxiv.

[7]  Trevor W Robbins,et al.  Appetitive Behavior , 2003, Annals of the New York Academy of Sciences.

[8]  A. Dickinson,et al.  The neuropsychological basis of addictive behaviour , 2001, Brain Research Reviews.

[9]  Z. M. Saygina,et al.  High-resolution magnetic resonance imaging reveals nuclei of the human amygdala : manual segmentation to automatic atlas , 2017 .

[10]  P. Södersten,et al.  Understanding eating disorders , 2006, Hormones and Behavior.

[11]  D. Amaral,et al.  Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study , 2002, The Journal of comparative neurology.

[12]  Jean-Baptiste Poline,et al.  Are fMRI event-related response constant in time? A model selection answer , 2006, NeuroImage.

[13]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[14]  A. McDonald.  Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[15]  E. Damianopoulos,et al.  A new proposal for drug conditioning with implications for drug addiction: The Pavlovian two-step from delay to trace conditioning , 2014, Behavioural Brain Research.

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

[17]  Ryan K. Jessup,et al.  Differentiable contributions of human amygdalar subregions in the computations underlying reward and avoidance learning , 2011, The European journal of neuroscience.

[18]  J. D. Nichols,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. , 1997, Science.

[19]  Michele Pignatelli,et al.  Antagonistic negative and positive neurons of the basolateral amygdala , 2016, Nature Neuroscience.

[20]  Joseph E LeDoux,et al.  The Contribution of the Amygdala to Aversive and Appetitive Pavlovian Processes , 2013 .

[21]  R. Stark,et al.  The 5‐HTTLPR polymorphism is associated with altered hemodynamic responses during appetitive conditioning , 2013, Human brain mapping.

[22]  Michelle M. Wedig,et al.  Differential amygdala habituation to neutral faces in young and elderly adults , 2005, Neuroscience Letters.

[23]  René Hurlemann,et al.  Segregating intra-amygdalar responses to dynamic facial emotion with cytoarchitectonic maximum probability maps , 2008, Journal of Neuroscience Methods.

[24]  Peter Bartel,et al.  Amygdala, affect and cognition: evidence from 10 patients with Urbach-Wiethe disease. , 2003, Brain : a journal of neurology.

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

[26]  K. Berridge,et al.  Which cue to ‘want’? Opioid stimulation of central amygdala makes goal-trackers show stronger goal-tracking, just as sign-trackers show stronger sign-tracking , 2012, Behavioural Brain Research.

[27]  Sharon L. Thompson-Schill,et al.  Item analysis in functional magnetic resonance imaging , 2007, NeuroImage.

[28]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[29]  A. Cybulska-Klosowicz.  Behavioral verification of associative learning in whiskers-related fear conditioning in mice. , 2016, Acta neurobiologiae experimentalis.

[30]  Tom Johnstone,et al.  Regional response differences across the human amygdaloid complex during social conditioning. , 2010, Cerebral cortex.

[31]  M. Keshavan,et al.  Reduced intra-amygdala activity to positively valenced faces in adolescent schizophrenia offspring , 2010, Schizophrenia Research.

[32]  Zachary A. Ingbretsen,et al.  Amygdala Responsivity to High-Level Social Information from Unseen Faces , 2014, The Journal of Neuroscience.

[33]  L. Lénárd,et al.  Positive reinforcing effect of oxytocin microinjection in the rat central nucleus of amygdala , 2016, Behavioural Brain Research.

[34]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[35]  Bruce Fischl,et al.  Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography , 2011, NeuroImage.

[36]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[37]  J. Parkinson,et al.  Autonomic arousal in an appetitive context in primates: a behavioural and neural analysis , 2005, The European journal of neuroscience.

[38]  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.

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

[40]  John C Gore,et al.  Functional connectivity‐based parcellation of amygdala using self‐organized mapping: A data driven approach , 2014, Human brain mapping.

[41]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[42]  T. Robbins,et al.  Dissociable roles of the central and basolateral amygdala in appetitive emotional learning , 2000, The European journal of neuroscience.

[43]  Peter Bossaerts,et al.  Evidence for Model-based Computations in the Human Amygdala during Pavlovian Conditioning , 2013, PLoS Comput. Biol..

[44]  Shani E. Ross,et al.  Deep brain stimulation in the central nucleus of the amygdala decreases ‘wanting’ and ‘liking’ of food rewards , 2016, The European journal of neuroscience.

[45]  J. Dreher,et al.  Cerebral correlates of salient prediction error for different rewards and punishments. , 2013, Cerebral cortex.

[46]  Ewelina Knapska,et al.  Differential involvement of the central amygdala in appetitive versus aversive learning. , 2006, Learning & memory.

[47]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[48]  S. Rauch,et al.  Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study , 2003, Brain Research Bulletin.

[49]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[50]  Mimi Liljeholm,et al.  Neural Correlates of Specific and General Pavlovian-to-Instrumental Transfer within Human Amygdalar Subregions: A High-Resolution fMRI Study , 2012, The Journal of Neuroscience.

[51]  Mortimer Mishkin,et al.  Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations , 1981, Behavioural Brain Research.

[52]  A. Brechmann,et al.  Learning‐dependent plasticity in human auditory cortex during appetitive operant conditioning , 2013, Human Brain Mapping.

[53]  Ewelina Knapska,et al.  Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. , 2007, Physiological reviews.

[54]  A. Dale,et al.  Brain Changes in Older Adults at Very Low Risk for Alzheimer's Disease , 2013, The Journal of Neuroscience.

[55]  Timothy E. J. Behrens,et al.  Deep and Superficial Amygdala Nuclei Projections Revealed In Vivo by Probabilistic Tractography , 2011, The Journal of Neuroscience.

[56]  Elisabeth A. Murray,et al.  Behavioral/systems/cognitive Selective Bilateral Amygdala Lesions in Rhesus Monkeys Fail to Disrupt Object Reversal Learning , 2022 .

[57]  P. Holland,et al.  Rats with basolateral amygdala lesions show normal increases in conditioned stimulus processing but reduced conditioned potentiation of eating. , 2001, Behavioral neuroscience.

[58]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[59]  Jennifer Urbano Blackford,et al.  A unique role for the human amygdala in novelty detection , 2010, NeuroImage.

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

[61]  Didier Grandjean,et al.  Amygdala subregions differentially respond and rapidly adapt to threatening voices , 2013, Cortex.

[62]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[63]  Jerzy Bodurka,et al.  Trait impulsivity is related to ventral ACC and amygdala activity during primary reward anticipation. , 2015, Social cognitive and affective neuroscience.

[64]  R. Passingham,et al.  Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). , 1981, Journal of comparative and physiological psychology.

[65]  L. Kaczmarek,et al.  Functional anatomy of neural circuits regulating fear and extinction , 2012, Proceedings of the National Academy of Sciences.

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

[67]  Andreas Schulze-Bonhage,et al.  Response Properties of Human Amygdala Subregions: Evidence Based on Functional MRI Combined with Probabilistic Anatomical Maps , 2007, PloS one.

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

[69]  H. Flor,et al.  Contextual fear conditioning in humans using feature-identical contexts , 2015, Neurobiology of Learning and Memory.

[70]  M. Treadway,et al.  Reward processing dysfunction in major depression, bipolar disorder and schizophrenia , 2015, Current opinion in psychiatry.

[71]  R. Bammer.  Basic principles of diffusion-weighted imaging. , 2003, European journal of radiology.

[72]  S. Tonegawa,et al.  Basolateral to Central Amygdala Neural Circuits for Appetitive Behaviors , 2017, Neuron.

[73]  Michela Gallagher,et al.  Amygdala central nucleus function is necessary for learning but not expression of conditioned visual orienting , 2004, The European journal of neuroscience.

[74]  Ewelina Knapska,et al.  Reward Learning Requires Activity of Matrix Metalloproteinase-9 in the Central Amygdala , 2013, The Journal of Neuroscience.

[75]  Roland N. Boubela,et al.  fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions , 2015, Scientific Reports.

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

[77]  Kent C. Berridge,et al.  What and when to “want”? Amygdala-based focusing of incentive salience upon sugar and sex , 2011, Psychopharmacology.

[78]  Paulo Eduardo Neves Ferreira Velho,et al.  Amygdalae calcifications associated with disease duration in lipoid proteinosis , 2006 .

[79]  Sylvia M. L. Cox,et al.  Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward , 2005, The Journal of Neuroscience.

[80]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[81]  R. J. Dolan,et al.  Parallel Neural Responses in Amygdala Subregions and Sensory Cortex during Implicit Fear Conditioning , 2001, NeuroImage.

[82]  Peter Kirsch,et al.  Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study , 2003, NeuroImage.

[83]  Bradford C. Dickerson,et al.  A reliable protocol for the manual segmentation of the human amygdala and its subregions using ultra-high resolution MRI , 2012, NeuroImage.

[84]  Theresa M. Desrochers,et al.  Two different lateral amygdala cell populations contribute to the initiation and storage of memory , 2001, Nature Neuroscience.

[85]  J. Kramer,et al.  Comparing Volume Loss in Neuroanatomical Regions of Emotion versus Regions of Cognition in Healthy Aging , 2016, PloS one.

[86]  D. Gaffan,et al.  Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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