The neural correlates of subjective pleasantness

Processing of subjective pleasantness is essential in daily life decision making, particularly in the context of cognitive and environmental factors. Pleasure is mediated by a neural network and this network has been suggested to be the biological basis of pleasure including a whole range of different modalities and domains of pleasantness. This quantitative meta-analysis of brain imaging data focuses on studies 1) based on correlations between self-reported judgements of pleasantness and brain regions and investigates whether 2) immediate (during scanning) versus subsequent judgements (after scanning) differ in brain activity. We investigated concurrence across 40 studies reporting brain regions correlated with self-reported judgements of subjective pleasantness (attractiveness, liking or beauty) by means of activation likelihood estimation (ALE). Positive correlates of subjective pleasantness were found in mOFC, ventromedial prefrontal cortex, left ventral striatum, pregenual cortex, right cerebellum, left thalamus and the mid cingulate cortex. Negative correlates were found in left precentral gyrus, right cerebellum and right inferior frontal gyrus. A comparison of studies with subjective pleasantness judgement during or after scanning revealed no significant differences in brain activation. We conclude that subjective pleasantness judgements are directly related to brain regions that have been described as part of the reward circuitry (mOFC, ventral striatum). The results suggest that the evaluation of likability or pleasure is an automatic process and that it is neither elicited nor enhanced by instructions to report the outcome of these judgements.

[1]  J. Panksepp,et al.  The neurobiology of positive emotions , 2006, Neuroscience & Biobehavioral Reviews.

[2]  P. Glimcher,et al.  The Neurobiology of Decision: Consensus and Controversy , 2009, Neuron.

[3]  Chantal Delon-Martin,et al.  fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender , 2003, NeuroImage.

[4]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[5]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[6]  E. Leibenluft,et al.  Mothers' neural activation in response to pictures of their children and other children , 2004, Biological Psychiatry.

[7]  Edmund T Rolls,et al.  Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain , 2007, The European journal of neuroscience.

[8]  E. Rolls,et al.  Taste‐olfactory convergence, and the representation of the pleasantness of flavour, in the human brain , 2003, The European journal of neuroscience.

[9]  E. Rolls,et al.  Value, Pleasure and Choice in the Ventral Prefrontal Cortex , 2022 .

[10]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[11]  Ulrich Kirk,et al.  The Neural Basis of Object-Context Relationships on Aesthetic Judgment , 2008, PloS one.

[12]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[13]  Fabian Grabenhorst,et al.  How Pleasant and Unpleasant Stimuli Combine in Different Brain Regions: Odor Mixtures , 2007, The Journal of Neuroscience.

[14]  Edmund T Rolls,et al.  Enhanced affective brain representations of chocolate in cravers vs. non‐cravers , 2007, The European journal of neuroscience.

[15]  Perrine Ruby,et al.  A relation between rest and the self in the brain? , 2003, Brain Research Reviews.

[16]  M. Posner.  The Brain and Emotion , 1999, Nature Medicine.

[17]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[18]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.

[19]  Roberto Cabeza,et al.  Remembering beauty: Roles of orbitofrontal and hippocampal regions in successful memory encoding of attractive faces , 2011, NeuroImage.

[20]  D Yves von Cramon,et al.  Tuning‐in to the beat: Aesthetic appreciation of musical rhythms correlates with a premotor activity boost , 2009, Human brain mapping.

[21]  Alan C. Evans,et al.  Changes in brain activity related to eating , 2001 .

[22]  Gustavo Deco,et al.  Choice, difficulty, and confidence in the brain , 2010, NeuroImage.

[23]  E. Epel,et al.  Black sheep get the blues: A psychobiological model of social rejection and depression , 2010, Neuroscience & Biobehavioral Reviews.

[24]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  A. D. Craig,et al.  Human feelings: why are some more aware than others? , 2004, Trends in Cognitive Sciences.

[26]  Y. Okamoto,et al.  Gender differences in brain activity toward unpleasant linguistic stimuli concerning interpersonal relationships: an fMRI study , 2005, European Archives of Psychiatry and Clinical Neuroscience.

[27]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[28]  Kyle S. Smith,et al.  Hedonic Hot Spots in the Brain , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[30]  J. O'Doherty,et al.  Human Medial Orbitofrontal Cortex Is Recruited during Experience of Imagined and Real Rewards Prescan Training , 2022 .

[31]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[32]  Takashi Tsukiura,et al.  Shared brain activity for aesthetic and moral judgments: implications for the Beauty-is-Good stereotype. , 2011, Social cognitive and affective neuroscience.

[33]  Antonio Rangel,et al.  Hypothetical and Real Choice Differentially Activate Common Valuation Areas , 2011, The Journal of Neuroscience.

[34]  William A. Cunningham,et al.  Orbitofrontal cortex provides cross-modal valuation of self-generated stimuli. , 2011, Social cognitive and affective neuroscience.

[35]  Yousuke Kawachi,et al.  Discrete cortical regions associated with the musical beauty of major and minor chords , 2008, Cognitive, affective & behavioral neuroscience.

[36]  Kyle S. Smith,et al.  Hedonic Hotspots: Generating Sensory Pleasure in the Brain , 2007 .

[37]  Oshin Vartanian,et al.  Neuroanatomical correlates of aesthetic preference for paintings , 2004, Neuroreport.

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

[39]  Christopher J. Fox,et al.  The contribution of the fusiform gyrus and superior temporal sulcus in processing facial attractiveness: Neuropsychological and neuroimaging evidence , 2008, Neuroscience.

[40]  Fabian Grabenhorst,et al.  Selective attention to affective value alters how the brain processes taste stimuli , 2008, The European journal of neuroscience.

[41]  Jin Fan,et al.  Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[42]  E. Brattico,et al.  Music and Emotions in the Brain: Familiarity Matters , 2011, PloS one.

[43]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[44]  Paolo Maria Rossini,et al.  Dynamics of male sexual arousal: distinct components of brain activation revealed by fMRI , 2005, NeuroImage.

[45]  Edmund T. Rolls,et al.  Warm pleasant feelings in the brain , 2008, NeuroImage.

[46]  Simon B. Eickhoff,et al.  Naturalizing aesthetics: Brain areas for aesthetic appraisal across sensory modalities , 2011, NeuroImage.

[47]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[48]  D. Perrett,et al.  Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness , 2003, Neuropsychologia.

[49]  A. Craig.  Forebrain emotional asymmetry: a neuroanatomical basis? , 2005, Trends in Cognitive Sciences.

[50]  E. Rolls,et al.  Human cortical responses to water in the mouth, and the effects of thirst. , 2003, Journal of neurophysiology.

[51]  C. Büchel,et al.  Neural representations of subjective reward value , 2010, Behavioural Brain Research.

[52]  Paul E. Downing,et al.  Neural Correlates of Appetite and Hunger-Related Evaluative Judgments , 2009, PloS one.

[53]  James M. Kilner,et al.  Brain systems for assessing facial attractiveness , 2007, Neuropsychologia.

[54]  Amy L. Thomas,et al.  The neural response to facial attractiveness. , 2009, Neuropsychology.

[55]  V. Michel,et al.  An Automatic Valuation System in the Human Brain: Evidence from Functional Neuroimaging , 2009, Neuron.

[56]  K. Ohtomo,et al.  Effect of the observed pupil size on the amygdala of the beholders. , 2012, Social cognitive and affective neuroscience.

[57]  Richard J. Davidson,et al.  PSYCHOLOGICAL SCIENCE Research Article Lending a Hand Social Regulation of the Neural Response to Threat , 2022 .

[58]  Paul J. Whalen,et al.  Are Attractive People Rewarding? Sex Differences in the Neural Substrates of Facial Attractiveness , 2008, Journal of Cognitive Neuroscience.

[59]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[60]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[61]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[62]  Alan C. Evans,et al.  Changes in brain activity related to eating chocolate: from pleasure to aversion. , 2001, Brain : a journal of neurology.

[63]  E. Rolls,et al.  How the brain represents the reward value of fat in the mouth. , 2010, Cerebral cortex.

[64]  D. Yves von Cramon,et al.  Corrigendum to “Brain correlates of aesthetic judgment of beauty” [NeuroImage 29 (2006) 276–285] , 2006, NeuroImage.

[65]  Á. Pascual-Leone,et al.  How do we modulate our emotions? Parametric fMRI reveals cortical midline structures as regions specifically involved in the processing of emotional valences. , 2005, Brain research. Cognitive brain research.

[66]  G. Rizzolatti,et al.  The Golden Beauty: Brain Response to Classical and Renaissance Sculptures , 2007, PloS one.

[67]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[68]  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.

[69]  J. O'Doherty,et al.  Predictive Neural Coding of Reward Preference Involves Dissociable Responses in Human Ventral Midbrain and Ventral Striatum , 2006, Neuron.

[70]  S. Zeki,et al.  Neural correlates of beauty. , 2004, Journal of neurophysiology.

[72]  J. O'Doherty,et al.  Marketing actions can modulate neural representations of experienced pleasantness , 2008, Proceedings of the National Academy of Sciences.

[73]  O. Bonne,et al.  Cerebral Activation Associated with Sexual Arousal in Response to a Pornographic Clip: A 15O–H2O PET Study in Heterosexual Men , 2001, NeuroImage.