Consolidation power of extrinsic rewards: reward cues enhance long-term memory for irrelevant past events.

Recent research suggests that extrinsic rewards promote memory consolidation through dopaminergic modulation processes. However, no conclusive behavioral evidence exists given that the influence of extrinsic reward on attention and motivation during encoding and consolidation processes are inherently confounded. The present study provides behavioral evidence that extrinsic rewards (i.e., monetary incentives) enhance human memory consolidation independently of attention and motivation. Participants saw neutral pictures, followed by a reward or control cue in an unrelated context. Our results (and a direct replication study) demonstrated that the reward cue predicted a retrograde enhancement of memory for the preceding neutral pictures. This retrograde effect was observed only after a delay, not immediately upon testing. An additional experiment showed that emotional arousal or unconscious resource mobilization cannot explain the retrograde enhancement effect. These results provide support for the notion that the dopaminergic memory consolidation effect can result from extrinsic reward.

[1]  A. Yonelinas Components of episodic memory: the contribution of recollection and familiarity. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  J. Cacioppo,et al.  Negative information weighs more heavily on the brain: The negativity bias in evaluative categorizations. , 1998 .

[3]  J. O'Doherty,et al.  Is Avoiding an Aversive Outcome Rewarding? Neural Substrates of Avoidance Learning in the Human Brain , 2006, PLoS biology.

[4]  Jeff T. Larsen,et al.  Negative information weighs more heavily on the brain: the negativity bias in evaluative categorizations. , 1998, Journal of personality and social psychology.

[5]  Roshan Cools,et al.  Dissociable responses to punishment in distinct striatal regions during reversal learning , 2010, NeuroImage.

[6]  W. F. Harley,et al.  The effect of monetary incentive in paired associate learning using a differential method , 1965 .

[7]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[8]  H. Aarts,et al.  Human Reward Pursuit , 2012 .

[9]  Martin P Paulus,et al.  Ventromedial prefrontal cortex activation is critical for preference judgments , 2003, Neuroreport.

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

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

[12]  J. Fell,et al.  Ventromedial Prefrontal Cortex Activation Is Associated with Memory Formation for Predictable Rewards , 2011, PloS one.

[13]  W. Honer,et al.  The impact of monetary reward on memory in schizophrenia spectrum disorder. , 2007, Neuropsychology.

[14]  D. Shohamy Learning and motivation in the human striatum , 2011, Current Opinion in Neurobiology.

[15]  Kou Murayama,et al.  Achievement Motivation and Memory : Achievement Goals Differentially Influence Immediate and Delayed Remember – Know Recognition Memory , 2011 .

[16]  M. Mather,et al.  Reconciling findings of emotion-induced memory enhancement and impairment of preceding items. , 2009, Emotion.

[17]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[18]  Elizabeth A. Phelps,et al.  How arousal modulates memory: Disentangling the effects of attention and retention , 2004, Cognitive, affective & behavioral neuroscience.

[19]  D. Shohamy,et al.  Dopamine and adaptive memory , 2010, Trends in Cognitive Sciences.

[20]  D. Wickens,et al.  Trace cue position, motivation, and short-term memory. , 1968, Journal of experimental psychology.

[21]  H. Heinze,et al.  Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation , 2005 .

[22]  Brian Knutson,et al.  Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation , 2006, Neuron.

[23]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[24]  Robert A. Bjork,et al.  The spacing effect: Consolidation or differential encoding? , 1970 .

[25]  Kenji Matsumoto,et al.  Neural basis of the undermining effect of monetary reward on intrinsic motivation , 2010, Proceedings of the National Academy of Sciences.

[26]  M. Schlund,et al.  Human avoidance and approach learning: Evidence for overlapping neural systems and experiential avoidance modulation of avoidance neurocircuitry , 2011, Behavioural Brain Research.

[27]  Alan D. Castel,et al.  The Adaptive and Strategic Use of Memory By Older Adults: Evaluative Processing and Value-Directed Remembering , 2007 .

[28]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[29]  R. Dantzer The Psychology of Fear and Stress, J.A. Gray (Ed.). Cambridge University Press, Cambridge (1987), viii and 422 pp, ISBN 0-521-27098-7 , 1989 .

[30]  B. Weiner Effects of motivations on the availability and retrieval of memory traces. , 1966 .

[31]  Andrew P. Yonelinas,et al.  Differential time-dependent effects of emotion on recollective experience and memory for contextual information , 2008, Cognition.

[32]  S. Lea,et al.  Money as tool, money as drug: The biological psychology of a strong incentive , 2006, Behavioral and Brain Sciences.

[33]  M. Mather,et al.  Positive Outcomes Enhance Incidental Learning for Both Younger and Older Adults , 2011, Front. Neurosci..

[34]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[35]  M. Guitart-Masip,et al.  NOvelty-related Motivation of Anticipation and exploration by Dopamine (NOMAD): Implications for healthy aging , 2010, Neuroscience & Biobehavioral Reviews.

[36]  Miranda R. Goode,et al.  Merely Activating the Concept of Money Changes Personal and Interpersonal Behavior , 2008 .

[37]  Peter Dayan,et al.  Hippocampal Contributions to Control: The Third Way , 2007, NIPS.

[38]  P. Montague,et al.  Neural Economics and the Biological Substrates of Valuation , 2002, Neuron.

[39]  H. Aarts,et al.  The Unconscious Eye Opener , 2009, Psychological science.

[40]  K. Murayama,et al.  Money enhances memory consolidation – But only for boring material , 2011, Cognition.

[41]  Henry L. Roediger,et al.  Enhancing Retention Through Reconsolidation , 2011, Psychological science.

[42]  P. Dayan,et al.  Serotonin in affective control. , 2009, Annual review of neuroscience.

[43]  John D E Gabrieli,et al.  Emotion enhances remembrance of neutral events past , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Mardi J. Horowitz,et al.  The Psychology of Fear and Stress, 2nd ed , 1989 .

[45]  N. Daw,et al.  Striatal Activity Underlies Novelty-Based Choice in Humans , 2008, Neuron.

[46]  P. Dayan,et al.  Reinforcement learning: The Good, The Bad and The Ugly , 2008, Current Opinion in Neurobiology.

[47]  Felix Breuer,et al.  Neural response to reward anticipation is modulated by Gray's impulsivity , 2009, NeuroImage.

[48]  E. Mori,et al.  Effects of emotion and reward motivation on neural correlates of episodic memory encoding: A PET study , 2010, Neuroscience Research.

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

[50]  Stephan Hamann,et al.  Cognitive and neural mechanisms of emotional memory , 2001, Trends in Cognitive Sciences.