Implicit motivational value and salience are processed in distinct areas of orbitofrontal cortex

Recent studies have shown that motivational stimulus information is represented in the brain even in situations where the individual is not actively engaged in stimulus evaluation. However, it has remained unclear whether neural representations of such implicit motivational information reflect the motivational value or motivational salience of stimuli. While motivational values correspond to the desirability of stimuli, motivational salience is related to the arousal elicited by the stimulus. Here we aimed at disentangling the neural representation of both motivational dimensions. In the first part, participants learned the association of face stimuli with monetary reward and punishment. The same face stimuli were presented in a subsequent fMRI experiment, during which participants either performed a gender discrimination task on the faces or an orientation discrimination task on two simultaneously presented bars. Importantly, faces only differed regarding their implicit motivational information as acquired in the previous learning task, as participants neither received monetary reinforcement during the fMRI experiment nor were they asked to explicitly judge their face preferences. We found that neural responses in lateral OFC were modulated by implicit motivational value, whereas the faces' implicit motivational salience was coded in medial OFC. While the value-related responses in lateral OFC decreased over time, the salience-related modulation of medial OFC activity remained stable over the duration of the fMRI experiment. Neural responses to both motivational dimensions were observed independent of whether participants' attention was directed to the faces or to the surrounding bars, suggesting an automatic processing of implicit motivational value and salience. The functional dissociation within the OFC suggests that this region is critically involved in distinct motivation-related processes: In medial OFC, a representation of salient items may be maintained in order to facilitate responses towards behaviourally relevant stimuli in the future; in contrast the temporary value effect in lateral OFC might reflect decreasing stimulus valuation in the absence of explicit motivational stimulus differences.

[1]  Patryk A. Laurent,et al.  Value-driven attentional capture , 2011, Proceedings of the National Academy of Sciences.

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

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

[4]  A. Rangel,et al.  Dissociating valuation and saliency signals during decision-making. , 2011, Cerebral cortex.

[5]  Denis Cousineau,et al.  Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method , 2005 .

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

[7]  M. Nicolelis,et al.  Neuronal Ensemble Bursting in the Basal Forebrain Encodes Salience Irrespective of Valence , 2008, Neuron.

[8]  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.

[9]  J. Raymond,et al.  Selective Visual Attention and Motivation , 2009, Psychological science.

[10]  Daniel C. Krawczyk,et al.  Reward modulation of prefrontal and visual association cortex during an incentive working memory task , 2007, Brain Research.

[11]  R. Dolan,et al.  The human amygdala and orbital prefrontal cortex in behavioural regulation , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[13]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

[14]  J. Driver,et al.  Rewarding Feedback After Correct Visual Discriminations Has Both General and Specific Influences on Visual Cortex , 2010, Journal of neurophysiology.

[15]  R. Dolan,et al.  Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value , 2004, Nature Neuroscience.

[16]  John T Serences,et al.  Value-Based Modulations in Human Visual Cortex , 2008, Neuron.

[17]  J. O'Doherty,et al.  Temporal isolation of neural processes underlying face preference decisions , 2007, Proceedings of the National Academy of Sciences.

[18]  J. Haynes,et al.  Neural Responses to Unattended Products Predict Later Consumer Choices , 2010, The Journal of Neuroscience.

[19]  S. Kapur,et al.  Separate brain regions code for salience vs. valence during reward prediction in humans , 2007, Human brain mapping.

[20]  C. Tallon-Baudry,et al.  Fast and Automatic Activation of an Abstract Representation of Money in the Human Ventral Visual Pathway , 2011, PloS one.

[21]  C. Daniel Salzman,et al.  The Convergence of Information about Rewarding and Aversive Stimuli in Single Neurons , 2009, The Journal of Neuroscience.

[22]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Antonio Rangel,et al.  Neural computations associated with goal-directed choice , 2010, Current Opinion in Neurobiology.

[24]  Lutz Jäncke,et al.  Individual preferences modulate incentive values: Evidence from functional MRI , 2008, Behavioral and Brain Functions.

[25]  P. Holland,et al.  Amygdala–frontal interactions and reward expectancy , 2004, Current Opinion in Neurobiology.

[26]  K. Saleem,et al.  Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey , 2008, The Journal of comparative neurology.

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

[28]  S. Ikemoto Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex , 2007, Brain Research Reviews.

[29]  Sylvia M. L. Cox,et al.  Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward , 2005, The Journal of Neuroscience.

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

[31]  E. Thorndike The law of effect. , 1927 .

[32]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

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

[34]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

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

[36]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

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

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

[39]  Colin Camerer,et al.  A framework for studying the neurobiology of value-based decision making , 2008, Nature Reviews Neuroscience.

[40]  R. Herrnstein On the law of effect. , 1970, Journal of the experimental analysis of behavior.

[41]  J. Wallis Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[42]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[43]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[44]  Moshe Bar,et al.  See it with feeling: affective predictions during object perception , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

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

[47]  Stephan Heckers,et al.  Further Evidence for Aberrant Prefrontal Salience Coding in Schizophrenia , 2010, Front. Behav. Neurosci..

[48]  L. Pessoa,et al.  Combined Effects of Attention and Motivation on Visual Task Performance: Transient and Sustained Motivational Effects , 2008, Front. Hum. Neurosci..

[49]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[50]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[51]  Brian Knutson,et al.  Valence and salience contribute to nucleus accumbens activation , 2008, NeuroImage.

[52]  M. Wessa,et al.  How to regulate emotion? Neural networks for reappraisal and distraction. , 2011, Cerebral cortex.

[53]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[54]  Jason P. Mitchell,et al.  Social Influence Modulates the Neural Computation of Value , 2011, Psychological science.

[55]  Simon B Eickhoff,et al.  Modulating the processing of emotional stimuli by cognitive demand. , 2012, Social cognitive and affective neuroscience.