Nucleus Accumbens and Medial Prefrontal Cortex Pleasure Rather Than Salience Activates Human

98: 1374–1379, 2007. Firstpublished June 27, 2007; doi:10.1152/jn.00230.2007. Recent humanfunctional imaging studies have linked the processing of pleasantvisual stimuli to activity in mesolimbic reward structures. However,whether the activation is driven specifically by the pleasantness of thestimulus, or by its salience, is unresolved. Here we find in two studiesthat free viewing of pleasant images of erotic and romantic couplesprompts clear, reliable increases in nucleus accumbens (NAc) andmedial prefrontal cortex (mPFC) activity, whereas equally arousing(salient) unpleasant images, and neutral pictures, do not. These datasuggest that in visual perception, the human NAc and mPFC arespecifically reactive to pleasant, rewarding stimuli and are not en-gaged by unpleasant stimuli, despite high stimulus salience.

[1]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

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

[3]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[4]  Helen E. Fisher,et al.  Romantic love: An fMRI study of a neural mechanism for mate choice , 2005, The Journal of comparative neurology.

[5]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[6]  M. Bradley,et al.  Startle Modification: Affect and the Startle Reflex , 1999 .

[7]  Heidi Johansen-Berg,et al.  Ventral Striatum/Nucleus Accumbens Activation to Smoking-Related Pictorial Cues in Smokers and Nonsmokers: A Functional Magnetic Resonance Imaging Study , 2005, Biological Psychiatry.

[8]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[9]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[10]  M. Bradley,et al.  Probing picture perception: activation and emotion. , 1996, Psychophysiology.

[11]  P. Lang,et al.  Emotion, motivation, and the brain: reflex foundations in animal and human research. , 2006, Progress in brain research.

[12]  Dean Sabatinelli,et al.  Affective picture perception: gender differences in visual cortex? , 2004, Neuroreport.

[13]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[14]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[15]  W. Schultz.  Predictive reward signal of dopamine neurons. , 1998, Journal of neurophysiology.

[16]  James M Kilner,et al.  Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala , 2005, The Journal of Neuroscience.

[17]  Helen E. Fisher,et al.  Reward, motivation, and emotion systems associated with early-stage intense romantic love. , 2005, Journal of neurophysiology.

[18]  J. Salamone,et al.  Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. , 2005, Current opinion in pharmacology.

[19]  Jennifer C. Britton,et al.  Neural correlates of social and nonsocial emotions: An fMRI study , 2006, NeuroImage.

[20]  Jens Frahm,et al.  COMMENTS AND CONTROVERSIES Functional MRI of the Human Amygdala , 2001 .

[21]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[22]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[23]  Jennifer C. Britton,et al.  Neural correlates of individual ratings of emotional salience: a trial-related fMRI study , 2004, NeuroImage.

[24]  Thomas J. Ross,et al.  Amygdala response to both positively and negatively valenced stimuli , 2001, Neuroreport.

[25]  Trevor W Robbins,et al.  Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): An anterograde and retrograde tract‐tracing study , 2007, The Journal of comparative neurology.

[26]  Christopher J Patrick,et al.  Effects of picture content and intensity on affective physiological response. , 2006, Psychophysiology.

[27]  Sven Joubert,et al.  Areas of brain activation in males and females during viewing of erotic film excerpts , 2002, Human brain mapping.

[28]  S. Quartz,et al.  Neural Differentiation of Expected Reward and Risk in Human Subcortical Structures , 2006, Neuron.

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

[30]  R. Dolan,et al.  Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans , 2006, Nature.

[31]  Niels Birbaumer,et al.  Gender differences in response to pictures of nudes: a magnetoencephalographic study , 2003, Biological Psychology.

[32]  Erick Janssen,et al.  Selecting Films for Sex Research: Gender Differences in Erotic Film Preference , 2003, Archives of sexual behavior.

[33]  S. Hamann,et al.  Men and women differ in amygdala response to visual sexual stimuli , 2004, Nature Neuroscience.

[34]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[35]  J. Price,et al.  Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks , 2000, The Journal of comparative neurology.

[36]  Paul Cumming,et al.  Net influx of plasma 6‐[18F]fluoro‐l‐DOPA (FDOPA) to the ventral striatum correlates with prefrontal processing of affective stimuli , 2006, The European journal of neuroscience.

[37]  M. Bradley,et al.  Emotional perception: correlation of functional MRI and event-related potentials. , 2006, Cerebral cortex.

[38]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[39]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[40]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[41]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[42]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[43]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Horvitz.  Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

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

[46]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

[47]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[48]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

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

[50]  Andreas Bartels,et al.  The neural correlates of maternal and romantic love , 2004, NeuroImage.