Behavioral/systems/cognitive Reward Changes Salience in Human Vision via the Anterior Cingulate

Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial. Theories of dopamine suggest that this reflects underlying biases in perception and attention, with reward enhancing the representation of reward-associated stimuli such that attention is more likely to be deployed to the location of these objects. Using measures of behavior and brain electricity in male and female humans, we demonstrate this to be the case. Sensory and perceptual processing of reward-associated visual features is facilitated such that attention is deployed to objects characterized by these features in subsequent experimental trials. This is the case even when participants know that a strategic decision to attend to reward-associated features will be counterproductive and result in suboptimal performance. Other results show that the magnitude of visual bias created by reward is predicted by the response to reward feedback in anterior cingulate cortex, an area with strong connections to dopaminergic structures in the midbrain. These results demonstrate that reward has an impact on vision that is independent of its role in the strategic establishment of endogenous attention. We suggest that reward acts to change visual salience and thus plays an important and undervalued role in attentional control.

[1]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[2]  M. Posner,et al.  Components of visual orienting , 1984 .

[3]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[4]  Susan L. Franzel,et al.  Guided search: an alternative to the feature integration model for visual search. , 1989, Journal of experimental psychology. Human perception and performance.

[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]  J. Theeuwes Cross-dimensional perceptual selectivity , 1991, Perception & psychophysics.

[7]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

[8]  P. Goldman-Rakic,et al.  Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. , 1993, Cerebral cortex.

[9]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.

[10]  S. Luck,et al.  Electrophysiological correlates of feature analysis during visual search. , 1994, Psychophysiology.

[11]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[12]  M. Rugg,et al.  Electrophysiology of Mind: Event-Related Brain Potentials and Cognition , 1995 .

[13]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

[14]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[15]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[17]  W. Smeets,et al.  Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians , 1998, Trends in Neurosciences.

[18]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[19]  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.

[20]  Geoffrey F. Woodman,et al.  Electrophysiological measurement of rapid shifts of attention during visual search , 1999, Nature.

[21]  M. Mesulam Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[23]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[24]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[25]  Clay B. Holroyd,et al.  Medial Prefrontal Cortex and Error Potentials , 2002, Science.

[26]  W. Schultz Getting Formal with Dopamine and Reward , 2002, Neuron.

[27]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[28]  Okihide Hikosaka,et al.  Reward-Dependent Gain and Bias of Visual Responses in Primate Superior Colliculus , 2003, Neuron.

[29]  R. Wise Dopamine, learning and motivation , 2004, Nature Reviews Neuroscience.

[30]  Michael J. Frank,et al.  By Carrot or by Stick: Cognitive Reinforcement Learning in Parkinsonism , 2004, Science.

[31]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[32]  S. Luck,et al.  Attention to Features Precedes Attention to Locations in Visual Search: Evidence from Electromagnetic Brain Responses in Humans , 2004, The Journal of Neuroscience.

[33]  J. Maunsell Neuronal representations of cognitive state: reward or attention? , 2004, Trends in Cognitive Sciences.

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

[35]  Michael Scherg,et al.  Functional imaging and localization of electromagnetic brain activity , 2005, Brain Topography.

[36]  Jan Theeuwes,et al.  Electrophysiological Evidence of the Capture of Visual Attention , 2013, J. Cogn. Neurosci..

[37]  Mark F Bear,et al.  Reward timing in the primary visual cortex. , 2006, Science.

[38]  L. Chelazzi,et al.  Visual Selective Attention and the Effects of Monetary Rewards , 2006, Psychological science.

[39]  J. Panksepp,et al.  Behavioral functions of the mesolimbic dopaminergic system: An affective neuroethological perspective , 2007, Brain Research Reviews.

[40]  L. Chelazzi,et al.  Learning to Attend and to Ignore Is a Matter of Gains and Losses , 2009, Psychological science.

[41]  Vincent Di Lollo,et al.  Electrophysiological Indices of Target and Distractor Processing in Visual Search , 2009, Journal of Cognitive Neuroscience.

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

[43]  Jon Driver,et al.  Reward Priority of Visual Target Singletons Modulates Event-Related Potential Signatures of Attentional Selection , 2009, Psychological science.

[44]  Pietro Perona,et al.  Homo economicus in visual search. , 2009, Journal of vision.

[45]  Ethan S. Bromberg-Martin,et al.  Midbrain Dopamine Neurons Signal Preference for Advance Information about Upcoming Rewards , 2009, Neuron.

[46]  Christopher J. Peck,et al.  Reward Modulates Attention Independently of Action Value in Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[47]  A. Pavlovic,et al.  The anterior cingulate cortex , 2009 .

[48]  Aaron R. Seitz,et al.  Dissociable Neural Effects of Long-term Stimulus–Reward Pairing in Macaque Visual Cortex , 2010, Journal of Cognitive Neuroscience.