Neural correlates of a ‘pessimistic’ attitude when anticipating events of unknown emotional valence

Since we do not know what future holds for us, we prepare for expected emotional events in order to deal with a pleasant or threatening environment. From an evolutionary perspective, it makes sense to be particularly prepared for the worst-case scenario. We were interested to evaluate whether this assumption is reflected in the central nervous information processing associated with expecting visual stimuli of unknown emotional valence. While being scanned with functional magnetic resonance imaging, healthy subjects were cued to expect and then perceive visual stimuli with a known emotional valence as pleasant, unpleasant, and neutral, as well as stimuli of unknown valence that could have been either pleasant or unpleasant. While anticipating pictures of unknown valence, the activity of emotion processing brain areas was similar to activity associated with expecting unpleasant pictures, but there were no areas in which the activity was similar to the activity when expecting pleasant pictures. The activity of the revealed regions, including bilateral insula, right inferior frontal gyrus, medial thalamus, and red nucleus, further correlated with the individual ratings of mood: the worse the mood, the higher the activity. These areas are supposedly involved in a network for internal adaptation and preparation processes in order to act according to potential or certain unpleasant events. Their activity appears to reflect a 'pessimistic' bias by anticipating the events of unknown valence to be unpleasant.

[1]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[2]  T. Dalgleish The emotional brain , 2004, Nature Reviews Neuroscience.

[3]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

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

[5]  T. Peters,et al.  Visualization of thalamic nuclei on high resolution, multi‐averaged T1 and T2 maps acquired at 1.5 T , 2005, Human brain mapping.

[6]  J. Decety,et al.  Neuroanatomical Correlates of Visually Evoked Sexual Arousal in Human Males , 1999, Archives of sexual behavior.

[7]  Patricia S Churchland,et al.  Self‐Representation in Nervous Systems , 2003, Annals of the New York Academy of Sciences.

[8]  A. J. Fridlund Evolution and facial action in reflex, social motive, and paralanguage , 1991, Biological Psychology.

[9]  Y. Okamoto,et al.  Brain activity during expectancy of emotional stimuli: an fMRI study , 2003, Neuroreport.

[10]  A R Gibson,et al.  Functional specialization within the cat red nucleus. , 2002, Journal of neurophysiology.

[11]  G. Ainslie Uncertainty as wealth , 2003, Behavioural Processes.

[12]  Paul J Laurienti,et al.  The subjective experience of pain: where expectations become reality. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Samuel R. Friedman,et al.  Depression: Clinical, Experimental, and Theoretical Aspects , 1968 .

[14]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

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

[16]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

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

[18]  M. Kimura,et al.  Complementary Process to Response Bias in the Centromedian Nucleus of the Thalamus , 2005, Science.

[19]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[20]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

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

[22]  A. Morel,et al.  Multiarchitectonic and stereotactic atlas of the human thalamus , 1997, The Journal of comparative neurology.

[23]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

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

[25]  H J Eysenck,et al.  The Orthogonality of Psychoticism and Neuroticism: A Factorial Study , 1971, Perceptual and motor skills.

[26]  Richard J. Davidson,et al.  Functional neuroanatomy of aversion and its anticipation , 2006, NeuroImage.

[27]  J. Gray Self-Rating and Eysenck Personality Inventory Estimates of Neuroticism and Extraversion , 1972, Psychological reports.

[28]  Karl J. Friston,et al.  Brain systems mediating aversive conditioning: An event related fMRI study , 1998, NeuroImage.

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

[30]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

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

[33]  Henrik Walter,et al.  Dissociating a Common Working Memory Network from Different Neural Substrates of Phonological and Spatial Stimulus Processing , 2002, NeuroImage.

[34]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  C. Darwin The Expression of the Emotions in Man and Animals , .

[36]  K. Luan Phan,et al.  Functional Neuroimaging Studies of Human Emotions , 2004, CNS Spectrums.

[37]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  G. Pagnoni,et al.  Explicit and Incidental Facial Expression Processing: An fMRI Study , 2001, NeuroImage.

[39]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Craig A. Smith,et al.  Patterns of cognitive appraisal in emotion. , 1985, Journal of personality and social psychology.

[41]  A. Beck Cognitive models of depression. , 1987 .

[42]  W. Lovallo,et al.  A comparison of four scales for anxiety, depresison, and neuroticism. , 1980, Journal of clinical psychology.

[43]  J. Armony,et al.  The influence of trait anxiety on autonomic response and cognitive performance during an anticipatory anxiety task , 2006, Depression and anxiety.

[44]  H. Mayberg Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. , 2003, British medical bulletin.

[45]  Dawn R. Collins,et al.  Reciprocal Changes in the Firing Probability of Lateral and Central Medial Amygdala Neurons , 1999, The Journal of Neuroscience.

[46]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[47]  S. Folkman,et al.  Appraisal, coping, health status, and psychological symptoms. , 1986, Journal of personality and social psychology.

[48]  Samuel M. McClure,et al.  The Neural Substrates of Reward Processing in Humans: The Modern Role of fMRI , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[49]  Henrik Walter,et al.  Expecting unpleasant stimuli – An fMRI study , 2007, Psychiatry Research: Neuroimaging.

[50]  M. Honda,et al.  Expectation of Pain Enhances Responses to Nonpainful Somatosensory Stimulation in the Anterior Cingulate Cortex and Parietal Operculum/Posterior Insula: an Event-Related Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[51]  H. Critchley,et al.  Neuroanatomical basis for first- and second-order representations of bodily states , 2001, Nature Neuroscience.

[52]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[53]  Justin S. Feinstein,et al.  Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. , 2005, Archives of general psychiatry.

[54]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[55]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[56]  J. Allman,et al.  A neuronal morphologic type unique to humans and great apes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Simmons,et al.  Anticipation of emotionally aversive visual stimuli activates right insula , 2004, Neuroreport.

[58]  Angelo Picardi,et al.  Stability of Alexithymia and Its Relationships with the ‘Big Five’ Factors, Temperament, Character, and Attachment Style , 2005, Psychotherapy and Psychosomatics.

[59]  C. Saper,et al.  Organization of visceral and limbic connections in the insular cortex of the rat , 1991, The Journal of comparative neurology.

[60]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[61]  Michael J. Anderle,et al.  The neural substrates of affective processing in depressed patients treated with venlafaxine. , 2003, The American journal of psychiatry.

[62]  R. Dolan,et al.  A Functional Anatomy of Anticipatory Anxiety , 1999, NeuroImage.

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

[64]  David C. Alsop,et al.  Dissociable networks for the expectancy and perception of emotional stimuli in the human brain , 2006, NeuroImage.

[65]  P. Lang The emotion probe. Studies of motivation and attention. , 1995, The American psychologist.

[66]  I. Tracey,et al.  Cortical processing of visceral and somatic stimulation: Differentiating pain intensity from unpleasantness , 2005, Neuroscience.

[67]  Jordan Grafman,et al.  Representation of attitudinal knowledge: role of prefrontal cortex, amygdala and parahippocampal gyrus , 2005, Neuropsychologia.

[68]  L. Heimer A new anatomical framework for neuropsychiatric disorders and drug abuse. , 2003, The American journal of psychiatry.

[69]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

[70]  A. Picardi,et al.  Stability of attachment-related anxiety and avoidance and their relationships with the five-factor model and the psychobiological model of personality. , 2005, Psychology and psychotherapy.

[71]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.