How Does Awareness Modulate Goal-Directed and Stimulus-Driven Shifts of Attention Triggered by Value Learning?

In order to behave adaptively, attention can be directed in space either voluntarily (i.e., endogenously) according to strategic goals, or involuntarily (i.e., exogenously) through reflexive capture by salient or novel events. The emotional or motivational value of stimuli can also strongly influence attentional orienting. However, little is known about how reward-related effects compete or interact with endogenous and exogenous attention mechanisms, particularly outside of awareness. Here we developed a visual search paradigm to study subliminal value-based attentional orienting. We systematically manipulated goal-directed or stimulus-driven attentional orienting and examined whether an irrelevant, but previously rewarded stimulus could compete with both types of spatial attention during search. Critically, reward was learned without conscious awareness in a preceding phase where one among several visual symbols was consistently paired with a subliminal monetary reinforcement cue. Our results demonstrated that symbols previously associated with a monetary reward received higher attentional priority in the subsequent visual search task, even though these stimuli and reward were no longer task-relevant, and despite reward being unconsciously acquired. Thus, motivational processes operating independent of conscious awareness may provide powerful influences on mechanisms of attentional selection, which could mitigate both stimulus-driven and goal-directed shifts of attention.

[1]  Juan Lupiáñez,et al.  Two cognitive and neural systems for endogenous and exogenous spatial attention , 2013, Behavioural Brain Research.

[2]  E. Fox.  Processing emotional facial expressions: The role of anxiety and awareness , 2002, Cognitive, affective & behavioral neuroscience.

[3]  Sarah Shomstein,et al.  Reward-Based Transfer From Bottom-Up to Top-Down Search Tasks , 2013, Psychological science.

[4]  Richard S. J. Frackowiak,et al.  Neurobiological measures of human selective attention , 2001, Neuropsychologia.

[5]  M. Peelen,et al.  Neural Mechanisms of Incentive Salience in Naturalistic Human Vision , 2015, Neuron.

[6]  H. Aarts,et al.  When unconscious rewards boost cognitive task performance inefficiently: the role of consciousness in integrating value and attainability information , 2012, Front. Hum. Neurosci..

[7]  S. Dehaene,et al.  Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework , 2001, Cognition.

[8]  Paolo Bartolomeo,et al.  Dorsal and Ventral Parietal Contributions to Spatial Orienting in the Human Brain , 2011, The Journal of Neuroscience.

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

[10]  H. Aarts,et al.  A new perspective on human reward research: How consciously and unconsciously perceived reward information influences performance , 2014, Cognitive, affective & behavioral neuroscience.

[11]  L. Chelazzi,et al.  Behavioral/systems/cognitive Reward Changes Salience in Human Vision via the Anterior Cingulate , 2022 .

[12]  L. Chelazzi,et al.  Altering Spatial Priority Maps via Reward-Based Learning , 2014, The Journal of Neuroscience.

[13]  A. Song,et al.  The involvement of the dopaminergic midbrain and cortico-striatal-thalamic circuits in the integration of reward prospect and attentional task demands. , 2012, Cerebral cortex.

[14]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[15]  S. Chipman.  The Remembered Present: A Biological Theory of Consciousness , 1990, Journal of Cognitive Neuroscience.

[16]  Patrik Vuilleumier,et al.  What makes your brain suggestible? Hypnotizability is associated with differential brain activity during attention outside hypnosis , 2015, NeuroImage.

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

[18]  Maurizio Corbetta,et al.  Distinct representations for shifts of spatial attention and changes of reward contingencies in the human brain , 2013, Cortex.

[19]  Patrik Vuilleumier,et al.  Affective and motivational control of vision. , 2015, Current opinion in neurology.

[20]  Steven Yantis,et al.  Reward predictions bias attentional selection , 2013, Front. Hum. Neurosci..

[21]  Harm Veling,et al.  Boosting or choking – How conscious and unconscious reward processing modulate the active maintenance of goal-relevant information , 2011, Consciousness and Cognition.

[22]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[23]  K. Nelissen,et al.  Dopaminergic Reward Signals Selectively Decrease fMRI Activity in Primate Visual Cortex , 2013, Neuron.

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

[25]  H. Aarts,et al.  Preparing and Motivating Behavior Outside of Awareness , 2008, Science.

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

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

[28]  Allen Allport,et al.  Visual attention , 1989 .

[29]  P. Vuilleumier,et al.  How does reward compete with goal-directed and stimulus-driven shifts of attention? , 2017, Cognition & emotion.

[30]  Steven Yantis,et al.  Value-driven attentional priority signals in human basal ganglia and visual cortex , 2014, Brain Research.

[31]  O. Hikosaka,et al.  Comparison of Reward Modulation in the Frontal Eye Field and Caudate of the Macaque , 2006, The Journal of Neuroscience.

[32]  W. Schultz.  Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[33]  Steven Yantis,et al.  Learned Value Magnifies Salience-Based Attentional Capture , 2011, PloS one.

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

[35]  W. Zoest,et al.  Reward-associated stimuli capture the eyes in spite of strategic attentional set , 2013, Vision Research.

[36]  Okihide Hikosaka,et al.  Positive and negative modulation of motor response in primate superior colliculus by reward expectation. , 2007, Journal of neurophysiology.

[37]  M. Vink,et al.  Distinct neural responses to conscious versus unconscious monetary reward cues , 2014, Human brain mapping.

[38]  H. Aarts,et al.  Unconscious reward cues increase invested effort, but do not change speed–accuracy tradeoffs , 2010, Cognition.

[39]  H. Aarts,et al.  The Unconscious Will: How the Pursuit of Goals Operates Outside of Conscious Awareness , 2010, Science.

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

[41]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[42]  P. Vuilleumier,et al.  Gambling against neglect: Unconscious spatial biases induced by reward reinforcement in healthy people and brain-damaged patients , 2013, Cortex.

[43]  P. Bartolomeo,et al.  Modulating the attentional bias in unilateral neglect: the effects of the strategic set , 2001, Experimental Brain Research.

[44]  Lesley K Fellows,et al.  Ventromedial Frontal Cortex Is Critical for Guiding Attention to Reward-Predictive Visual Features in Humans , 2015, The Journal of Neuroscience.

[45]  O. Hikosaka,et al.  The Primate Ventral Pallidum Encodes Expected Reward Value and Regulates Motor Action , 2012, Neuron.

[46]  P. Bartolomeo,et al.  Cortical control of inhibition of return: Causal evidence for task-dependent modulations by dorsal and ventral parietal regions , 2013, Cortex.