Early detection of intentional harm in the human amygdala.

A decisive element of moral cognition is the detection of harm and its assessment as intentional or unintentional. Moral cognition engages brain networks supporting mentalizing, intentionality, empathic concern and evaluation. These networks rely on the amygdala as a critical hub, likely through frontotemporal connections indexing stimulus salience. We assessed inferences about perceived harm using a paradigm validated through functional magnetic resonance imaging, eye-tracking and electroencephalogram recordings. During the task, we measured local field potentials in three patients with depth electrodes (n = 115) placed in the amygdala and in several frontal, temporal, and parietal locations. Direct electrophysiological recordings demonstrate that intentional harm induces early activity in the amygdala (<200 ms), which--in turn--predicts intention attribution. The amygdala was the only site that systematically discriminated between critical conditions and predicted their classification of events as intentional. Moreover, connectivity analysis showed that intentional harm induced stronger frontotemporal information sharing at early stages. Results support the 'many roads' view of the amygdala and highlight its role in the rapid encoding of intention and salience--critical components of mentalizing and moral evaluation.

[1]  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.

[2]  Jorge Moll,et al.  Social attachment and aversion in human moral cognition , 2009, Neuroscience & Biobehavioral Reviews.

[3]  Facundo Manes,et al.  Contextual social cognition and the behavioral variant of frontotemporal dementia , 2012, Neurology.

[4]  Michal Mikl,et al.  Neural correlates of affective picture processing — A depth ERP study , 2009, NeuroImage.

[5]  P. Ryvlin,et al.  Evoked potential study of hippocampal efferent projections in the human brain , 2011, Clinical Neurophysiology.

[6]  Jean Decety,et al.  The speed of morality: a high-density electrical neuroimaging study. , 2012, Journal of neurophysiology.

[7]  M. Baulac,et al.  An Intracranial EEG Study of the Neural Dynamics of Musical Valence Processing. , 2015, Cerebral cortex.

[8]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[9]  Christopher L. Asplund,et al.  Corticolimbic gating of emotion-driven punishment , 2014, Nature Neuroscience.

[10]  S. Dehaene,et al.  A direct intracranial record of emotions evoked by subliminal words. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[12]  J. Decety,et al.  Brain signatures of moral sensitivity in adolescents with early social deprivation , 2014, Scientific Reports.

[13]  J. Decety,et al.  The complex relation between morality and empathy , 2014, Trends in Cognitive Sciences.

[14]  J. Grafman,et al.  The neural basis of human moral cognition , 2005, Nature Reviews Neuroscience.

[15]  John W. Tukey,et al.  Exploratory Data Analysis. , 1979 .

[16]  A. Ibanez,et al.  Motor-language coupling: Direct evidence from early Parkinson’s disease and intracranial cortical recordings , 2013, Cortex.

[17]  François Mauguière,et al.  Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex A Depth Electrode ERP Study in Human , 2004, Neuron.

[18]  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.

[19]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[20]  S. Fiske,et al.  Perceived intent motivates people to magnify observed harms , 2015, Proceedings of the National Academy of Sciences.

[21]  B. Foster,et al.  Intrinsic and Task-Dependent Coupling of Neuronal Population Activity in Human Parietal Cortex , 2015, Neuron.

[22]  R. Saxe,et al.  The neural basis of the interaction between theory of mind and moral judgment , 2007, Proceedings of the National Academy of Sciences.

[23]  S. Dehaene,et al.  Information Sharing in the Brain Indexes Consciousness in Noncommunicative Patients , 2013, Current Biology.

[24]  J. Gross Analytical methods and experimental approaches for electrophysiological studies of brain oscillations , 2014, Journal of Neuroscience Methods.

[25]  K. Tye,et al.  From circuits to behaviour in the amygdala , 2015, Nature.

[26]  Katherine D. Kinzler,et al.  The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. , 2012, Cerebral cortex.

[27]  Alberto Priori,et al.  Functional and clinical neuroanatomy of morality. , 2012, Brain : a journal of neurology.

[28]  R. Adolphs,et al.  Electrophysiological Responses in the Human Amygdala Discriminate Emotion Categories of Complex Visual Stimuli , 2002, The Journal of Neuroscience.

[29]  Michael J. Kahana,et al.  Direct brain recordings fuel advances in cognitive electrophysiology , 2010, Trends in Cognitive Sciences.

[30]  M. Hauser,et al.  The role of emotion in moral psychology , 2009, Trends in Cognitive Sciences.

[31]  J. Grafman,et al.  Opinion: the neural basis of human moral cognition. , 2005, Nature reviews. Neuroscience.