Current Emotion Research in Behavioral Neuroscience: The Role(s) of the Amygdala

Substantial advances in our understanding of the neural bases of emotional processing have been made over the past decades. Overall, studies in humans and other animals highlight the key role of the amygdala in the detection and evaluation of stimuli with affective value. Nonetheless, contradictory findings have been reported, especially in terms of the exact role of this structure in the processing of different emotions, giving rise to different neural models of emotion. For instance, although the amygdala has traditionally been considered as exclusively involved in fear (and possibly anger), more recent work suggests that it may be important for processing other types of emotions, and even nonemotional information. A review of the main findings in this field is presented here, together with some of the hypotheses that have been put forward to interpret this literature and explain its inconsistencies.

[1]  Nikos K. Logothetis,et al.  Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala , 2007, Current Biology.

[2]  A. Pitkänen,et al.  Comparison of the distribution of calcium-binding proteins and intrinsic connectivity in the lateral nucleus of the rat, monkey, and human amygdala , 2002, Pharmacology Biochemistry and Behavior.

[3]  K. Scherer,et al.  Acoustic profiles in vocal emotion expression. , 1996, Journal of personality and social psychology.

[4]  I. Peretz,et al.  Impaired recognition of musical emotions and facial expressions following anteromedial temporal lobe excision , 2011, Cortex.

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

[6]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  D. Gentile,et al.  Infants' discrimination of happy and sad music. , 2008, Infant behavior & development.

[8]  T. H. Brown,et al.  Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala , 2012, Behavioural Brain Research.

[9]  Joseph E LeDoux,et al.  Cells in the posterior thalamus project to both amygdala and temporal cortex: A quantitative retrograde double‐labeling study in the rat , 2000, The Journal of comparative neurology.

[10]  P Vuilleumier,et al.  Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect , 2002, Neuropsychologia.

[11]  P. Laukka,et al.  Impact of intended emotion intensity on cue utilization and decoding accuracy in vocal expression of emotion. , 2000, Emotion.

[12]  Sanger Brown,et al.  An Investigation into the Functions of the Occipital and Temporal Lobes of the Monkey's Brain , 1888 .

[13]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[14]  D. Blanchard,et al.  Innate and conditioned reactions to threat in rats with amygdaloid lesions. , 1972, Journal of comparative and physiological psychology.

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

[16]  D. Purves,et al.  Expression of Emotion in Eastern and Western Music Mirrors Vocalization , 2012, PloS one.

[17]  Alexander Todorov,et al.  Nonlinear Amygdala Response to Face Trustworthiness: Contributions of High and Low Spatial Frequency Information , 2009, Journal of Cognitive Neuroscience.

[18]  G. Schlaug,et al.  Amygdala activity can be modulated by unexpected chord functions during music listening , 2008, Neuroreport.

[19]  D. Wildgruber,et al.  Emotional voices in context: a neurobiological model of multimodal affective information processing. , 2011, Physics of life reviews.

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

[21]  Gregory J. Quirk,et al.  Prefrontal Mechanisms in Extinction of Conditioned Fear , 2006, Biological Psychiatry.

[22]  O. A. Andreassen,et al.  The human amygdala is involved in general behavioral relevance detection: Evidence from an event-related functional magnetic resonance imaging Go-NoGo task , 2008, Neuroscience.

[23]  J. Armony,et al.  Self-relevance modulates brain responses to angry body expressions , 2013, Cortex.

[24]  D. Davies,et al.  The Effects of Archistriatal Lesions on One‐trial Passive Avoidance Learning in the Chick , 1994, The European journal of neuroscience.

[25]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[27]  R. Adolphs,et al.  Amygdala damage impairs emotion recognition from music , 2007, Neuropsychologia.

[28]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

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

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

[31]  Joseph E. LeDoux,et al.  Aversive learning in patients with unilateral lesions of the amygdala and hippocampus , 2001, Biological Psychology.

[32]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[33]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Elizabeth K. Johnson,et al.  Statistical learning of tone sequences by human infants and adults , 1999, Cognition.

[35]  Josef Syka,et al.  Effect of auditory cortex lesions on the discrimination of frequency‐modulated tones in rats , 2006, The European journal of neuroscience.

[36]  E. Phelps,et al.  Social learning of fear , 2007, Nature Neuroscience.

[37]  Joseph E LeDoux,et al.  Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. , 1997, Cerebral cortex.

[38]  H. Ursin,et al.  Corticosterone and avoidance in rats with basolateral amygdala lesions. , 1973, Journal of comparative and physiological psychology.

[39]  Sophie K. Scott,et al.  Impaired auditory recognition of fear and anger following bilateral amygdala lesions , 1997, Nature.

[40]  K. Perryman,et al.  Slow wave changes in amygdala to visual, auditory, and social stimuli following lesions of the inferior temporal cortex in squirrel monkey (Saimiri sciureus). , 1987, Behavioral and neural biology.

[41]  Erin W. Dickie,et al.  Amygdala responses to unattended fearful faces: Interaction between sex and trait anxiety , 2008, Psychiatry Research: Neuroimaging.

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

[43]  Hanna Damasio,et al.  Neural systems for recognition of emotional prosody: a 3-D lesion study. , 2002, Emotion.

[44]  Isabelle Peretz,et al.  Role of tempo entrainment in psychophysiological differentiation of happy and sad music? , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[45]  Joseph E LeDoux,et al.  Somatosensory and auditory convergence in the lateral nucleus of the amygdala. , 1993, Behavioral neuroscience.

[46]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[47]  Eckart Altenmüller,et al.  Evolution of Emotional Communication: From Sounds in Nonhuman Mammals to Speech and Music in Man , 2013 .

[48]  N. Costes,et al.  Emotional Responses to Pleasant and Unpleasant Olfactory, Visual, and Auditory Stimuli: a Positron Emission Tomography Study , 2000, The Journal of Neuroscience.

[49]  Fred J Helmstetter,et al.  Human amygdala activity during the expression of fear responses. , 2006, Behavioral neuroscience.

[50]  Steven C. R. Williams,et al.  A functional MRI study of happy and sad affective states induced by classical music , 2007, Human brain mapping.

[51]  Lisa M. Shin,et al.  Neurocircuitry Models of Posttraumatic Stress Disorder and Extinction: Human Neuroimaging Research—Past, Present, and Future , 2006, Biological Psychiatry.

[52]  Jennifer A. Hobin,et al.  Auditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning Mnemonic Code or Fear Bias? , 2003, Neuron.

[53]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  B. Gelder Towards the neurobiology of emotional body language , 2006, Nature Reviews Neuroscience.

[55]  C. P. Heinlein The affective characters of the major and minor modes in music. , 1928 .

[56]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[57]  J. Johnston Further contributions to the study of the evolution of the forebrain , 1923 .

[58]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[59]  H. Klüver,et al.  PRELIMINARY ANALYSIS OF FUNCTIONS OF THE TEMPORAL LOBES IN MONKEYS , 1939 .

[60]  S. Scott,et al.  Saying it with feeling: neural responses to emotional vocalizations , 1999, Neuropsychologia.

[61]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[62]  D. Amaral,et al.  The Development of Social Behavior Following Neonatal Amygdala Lesions in Rhesus Monkeys , 2004, Journal of Cognitive Neuroscience.

[63]  H Scheich,et al.  Auditory perception of laughing and crying activates human amygdala regardless of attentional state. , 2001, Brain research. Cognitive brain research.

[64]  A. Young,et al.  Recognition of facial emotion in nine individuals with bilateral amygdala damage , 1999, Neuropsychologia.

[65]  David G. Amaral,et al.  Neuroanatomy of the primate amygdala. , 2009 .

[66]  J. Bachevalier,et al.  Impact of amygdala, orbital frontal, or hippocampal lesions on threat avoidance and emotional reactivity in nonhuman primates. , 2009, Emotion.

[67]  M. Baulac,et al.  Multidimensional scaling of emotional responses to music in patients with temporal lobe resection , 2011, Cortex.

[68]  Joseph E. LeDoux,et al.  Oxford Handbook of Auditory Science The Auditory Brain , 2012 .

[69]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[70]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  Daniel Tranel,et al.  Intact recognition of emotional prosody following amygdala damage , 1999, Neuropsychologia.

[72]  K. Scherer Expression of emotion in voice and music. , 1995, Journal of voice : official journal of the Voice Foundation.

[73]  D Yves von Cramon,et al.  Distinct fMRI responses to laughter, speech, and sounds along the human peri-sylvian cortex. , 2005, Brain research. Cognitive brain research.

[74]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

[75]  A K Anderson,et al.  Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. , 1998, Neuroreport.

[76]  E. Rolls,et al.  Neurons in the amygdala of the monkey with responses selective for faces , 1985, Behavioural Brain Research.

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

[78]  G. Pourtois,et al.  Perception of Facial Expressions and Voices and of their Combination in the Human Brain , 2005, Cortex.

[79]  J. Delgado,et al.  AMYGDALA UNITARY ACTIVITY IN THE UNRESTRAINED CAT. , 1963, Electroencephalography and clinical neurophysiology.

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

[81]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

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

[83]  L. Weiskrantz,et al.  Behavioral changes associated with ablation of the amygdaloid complex in monkeys. , 1956, Journal of comparative and physiological psychology.

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

[85]  A. Friederici,et al.  Investigating emotion with music: An fMRI study , 2006, Human brain mapping.

[86]  D. Hasboun,et al.  Impaired recognition of fear in voices and reduced anxiety after unilateral temporal lobe resection , 2011, Neuropsychologia.

[87]  J. Bachevalier,et al.  The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). , 2006, Behavioral neuroscience.

[88]  Didier Grandjean,et al.  Specific brain networks during explicit and implicit decoding of emotional prosody. , 2012, Cerebral cortex.

[89]  Pascal Belin,et al.  Amygdala responses to nonlinguistic emotional vocalizations , 2007, NeuroImage.

[90]  Swann Pichon,et al.  Two different faces of threat. Comparing the neural systems for recognizing fear and anger in dynamic body expressions , 2009, NeuroImage.

[91]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[92]  Katsuki Nakamura,et al.  Responses of single neurons in monkey amygdala to facial and vocal emotions. , 2007, Journal of neurophysiology.

[93]  H Nishijo,et al.  Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  Daniel C. Javitt,et al.  “It's Not What You Say, But How You Say it”: A Reciprocal Temporo-frontal Network for Affective Prosody , 2009, Front. Hum. Neurosci..

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

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

[97]  Joseph E LeDoux,et al.  NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala , 1995, Experimental Brain Research.

[98]  Joseph E LeDoux,et al.  Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[99]  Swann Pichon,et al.  Threat prompts defensive brain responses independently of attentional control. , 2012, Cerebral cortex.

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

[101]  B. Torres,et al.  Avoidance Response in Goldfish: Emotional and Temporal Involvement of Medial and Lateral Telencephalic Pallium , 2004, The Journal of Neuroscience.

[102]  W. Paesschen,et al.  Classically conditioned fear responses are preserved following unilateral temporal lobectomy in humans when concurrent US-expectancy ratings are used , 2009, Neuropsychologia.

[103]  Karine Sergerie,et al.  The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies , 2008, Neuroscience & Biobehavioral Reviews.

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

[105]  R. M. Siegel,et al.  Lack of selectivity for simple shapes defined by motion and luminance in STPa of the behaving macaque , 1998, Neuroreport.

[106]  Gilles Pourtois,et al.  Emotion and attention interactions in social cognition: Brain regions involved in processing anger prosody , 2005, NeuroImage.

[107]  Patrik Vuilleumier,et al.  Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity. , 2009, Emotion.

[108]  Peter A. Bandettini,et al.  The role of the human amygdala in the production of conditioned fear responses , 2005, NeuroImage.

[109]  Gilles Pourtois,et al.  Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy , 2010, Cognitive, affective & behavioral neuroscience.

[110]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[111]  S. Shelton,et al.  The Role of the Central Nucleus of the Amygdala in Mediating Fear and Anxiety in the Primate , 2004, The Journal of Neuroscience.

[112]  S Imaizumi,et al.  Observation of neural processes of auditory scene analysis by magnetoencephalography. , 1997, Acta oto-laryngologica. Supplementum.

[113]  Fabio Sambataro,et al.  Preferential responses in amygdala and insula during presentation of facial contempt and disgust , 2006, The European journal of neuroscience.

[114]  R. Adolphs,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans , 1995, Science.

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

[116]  Joseph E LeDoux,et al.  Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. , 1996, Learning & memory.

[117]  S. Koelsch Towards a neural basis of music-evoked emotions , 2010, Trends in Cognitive Sciences.