Neural mechanisms underlying the reward‐related enhancement of motivation when remembering episodic memories with high difficulty

The motivation to receive rewards enhances episodic memories, and the motivation is modulated by task difficulty. In episodic retrieval, however, functional neuroimaging evidence regarding the motivation that mediates interactions between reward and task difficulty is scarce. The present fMRI study investigated this issue. During encoding performed without fMRI, participants encoded Japanese words using either deep or shallow strategies, which led to variation in difficulty level during subsequent retrieval. During retrieval with fMRI, participants recognized the target words in either high or low monetary reward conditions. In the behavioral results, a reward‐related enhancement of memory was found only when the memory retrieval was difficult, and the rewarding effect on subjective motivation was greater in the retrieval of memories with high difficulty than those with low difficulty. The fMRI data showed that reward‐related increases in the activation of the substantia nigra/ventral tegmental area (SN/VTA), medial temporal lobe (MTL), dorsomedial prefrontal cortex (dmPFC), and dorsolateral prefrontal cortex (dlPFC) were greater during the retrieval of memories with high difficulty than those with low difficulty. Furthermore, reward‐related enhancement of functional connectivity between the SN/VTA and MTL and between the SN/VTA and dmPFC during the retrieval of memories with high difficulty was significantly correlated with reward‐related increases of retrieval accuracy and subjective motivation. The reward‐related enhancement of episodic retrieval and retrieval‐related motivation could be most effective when the level of retrieval difficulty is optimized. Such reward‐related enhancement of memory and motivation could be modulated by a network including the reward‐related SN/VTA, motivation‐related dmPFC, and memory‐related MTL. Hum Brain Mapp 38:3428–3443, 2017. © 2017 Wiley Periodicals, Inc.

[1]  R. Ryan,et al.  Relation of reward contingency and interpersonal context to intrinsic motivation: A review and test using cognitive evaluation theory. , 1983 .

[2]  Matthew B. Wall,et al.  Time perception: Manipulation of task difficulty dissociates clock functions from other cognitive demands , 2007, Neuropsychologia.

[3]  Jérôme Prado,et al.  Overcoming Perceptual Features in Logical Reasoning: A Parametric Functional Magnetic Resonance Imaging Study , 2007, Journal of Cognitive Neuroscience.

[4]  R. Yerkes,et al.  The relation of strength of stimulus to rapidity of habit‐formation , 1908 .

[5]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[6]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[7]  Christina E. Shalley,et al.  Effects of Goal Difficulty and Expected External Evaluation on Intrinsic Motivation: A Laboratory Study , 1985 .

[8]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[9]  P. Dayan,et al.  Effort and Valuation in the Brain: The Effects of Anticipation and Execution , 2013, The Journal of Neuroscience.

[10]  F. Craik,et al.  Depth of processing and the retention of words , 1975 .

[11]  C. N. Boehler,et al.  Task-Load-Dependent Activation of Dopaminergic Midbrain Areas in the Absence of Reward , 2011, The Journal of Neuroscience.

[12]  E. Duffy,et al.  The psychological significance of the concept of arousal or activation. , 1957, Psychological review.

[13]  Lila Davachi,et al.  Selective and Shared Contributions of the Hippocampus and Perirhinal Cortex to Episodic Item and Associative Encoding , 2008, Journal of Cognitive Neuroscience.

[14]  Theodore D. Satterthwaite,et al.  Dissociable but inter-related systems of cognitive control and reward during decision making: Evidence from pupillometry and event-related fMRI , 2007, NeuroImage.

[15]  Susanne M. Jaeggi,et al.  Does excessive memory load attenuate activation in the prefrontal cortex? Load-dependent processing in single and dual tasks: functional magnetic resonance imaging study , 2003, NeuroImage.

[16]  P. Haggard Human volition: towards a neuroscience of will , 2008, Nature Reviews Neuroscience.

[17]  M. Morgan Reward-Induced Decrements and Increments in Intrinsic Motivation , 1984 .

[18]  E. Düzel,et al.  The novelty exploration bonus and its attentional modulation , 2009, Neuropsychologia.

[19]  S. Shimojo,et al.  Neural Mechanisms Underlying Paradoxical Performance for Monetary Incentives Are Driven by Loss Aversion , 2012, Neuron.

[20]  Kaia L. Vilberg,et al.  Motivated Memories: Effects of Reward and Recollection in the Core Recollection Network and Beyond. , 2015, Cerebral cortex.

[21]  Ryuta Kawashima,et al.  Remembering with Gains and Losses: Effects of Monetary Reward and Punishment on Successful Encoding Activation of Source Memories , 2013, Cerebral cortex.

[22]  Scott A. Huettel,et al.  Resting state networks distinguish human ventral tegmental area from substantia nigra , 2014, NeuroImage.

[23]  Hoi-Chung Leung,et al.  Load response functions in the human spatial working memory circuit during location memory updating , 2007, NeuroImage.

[24]  Daniel G Dillon,et al.  Weak reward source memory in depression reflects blunted activation of VTA/SN and parahippocampus. , 2014, Social cognitive and affective neuroscience.

[25]  Samuel M. McClure,et al.  BOLD Responses Reflecting Dopaminergic Signals in the Human Ventral Tegmental Area , 2008, Science.

[26]  H. Walter,et al.  The relationship between level of processing and hippocampal–cortical functional connectivity during episodic memory formation in humans , 2013, Human brain mapping.

[27]  C. H. Donahue,et al.  Dynamic Routing of Task-relevant Signals for Decision Making in Dorsolateral Prefrontal Cortex , 2015, Nature Neuroscience.

[28]  Rewards, Task Difficulty, and Intrinsic Motivation: A Test of Learned Industriousness Theory , 2004 .

[29]  Hannah S. Locke,et al.  Prefrontal cortex mediation of cognitive enhancement in rewarding motivational contexts , 2010, Proceedings of the National Academy of Sciences.

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

[31]  E. Deci Effects of Externally Mediated Rewards on Intrinsic Motivation. , 1971 .

[32]  Soyoung Q. Park,et al.  Neural Integration of Risk and Effort Costs by the Frontal Pole: Only upon Request , 2013, The Journal of Neuroscience.

[33]  Sandra E Black,et al.  fMRI differences in encoding and retrieval of pictures due to encoding strategy in the elderly , 2004, Human brain mapping.

[34]  S. Nicola,et al.  Contributions of the amygdala and medial prefrontal cortex to incentive cue responding , 2008, Neuroscience.

[35]  S. Rombouts,et al.  Brain regions involved in the learning and application of reward rules in a two-deck gambling task , 2010, Neuropsychologia.

[36]  R B MALMO,et al.  Activation: a neuropsychological dimension. , 1959, Rassegna giuliana di medicina.

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

[38]  J B Poline,et al.  The neural system that bridges reward and cognition in humans: An fMRI study , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Raghu Nath,et al.  Role of Performance Goals in Prose Learning. , 1976 .

[40]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[41]  S. Hanson,et al.  Dynamic changes in the medial temporal lobe during incidental learning of object-location associations. , 2012, Cerebral cortex.

[42]  K. Luan Phan,et al.  A functional neuroimaging study of motivation and executive function , 2004, NeuroImage.

[43]  B M Gaymard,et al.  Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. , 2000, Cerebral cortex.

[44]  Effects of Task Difficulty on Subsequent Preference for Visual Complexity , 1975, Perceptual and motor skills.

[45]  Lila Davachi,et al.  Object Unitization and Associative Memory Formation Are Supported by Distinct Brain Regions , 2010, The Journal of Neuroscience.

[46]  R. Nisbett,et al.  Undermining children's intrinsic interest with extrinsic reward: A test of the "overjustification" hypothesis. , 1973 .

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

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

[49]  D. Hebb Drives and the C.N.S. (conceptual nervous system). , 1955, Psychological review.

[50]  Qiang Wang,et al.  Distributed Value Representation in the Medial Prefrontal Cortex during Intertemporal Choices , 2014, The Journal of Neuroscience.

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

[52]  Alison R. Preston,et al.  Reward Modulation of Hippocampal Subfield Activation during Successful Associative Encoding and Retrieval , 2012, Journal of Cognitive Neuroscience.

[53]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[54]  Sanghoon Han,et al.  Isolating rule- versus evidence-based prefrontal activity during episodic and lexical discrimination: a functional magnetic resonance imaging investigation of detection theory distinctions. , 2005, Cerebral cortex.

[55]  V. Stuphorn,et al.  Medial Frontal Cortex Motivates But Does Not Control Movement Initiation in the Countermanding Task , 2010, The Journal of Neuroscience.

[56]  Michael W. Cole,et al.  Reward Motivation Enhances Task Coding in Frontoparietal Cortex. , 2016, Cerebral cortex.

[57]  H. L. Hom,et al.  The impact of task difficulty expectations on intrinsic motivation , 1983 .

[58]  Michael D. Rugg,et al.  Further Dissociating the Processes Involved in Recognition Memory: An fMRI Study , 2005, Journal of Cognitive Neuroscience.

[59]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[60]  S. Nicola,et al.  Dorsomedial Prefrontal Cortex Contribution to Behavioral and Nucleus Accumbens Neuronal Responses to Incentive Cues , 2008, The Journal of Neuroscience.

[61]  H. Heinze,et al.  Reward-Related fMRI Activation of Dopaminergic Midbrain Is Associated with Enhanced Hippocampus- Dependent Long-Term Memory Formation , 2005, Neuron.

[62]  Alex Martin,et al.  Access the most recent version at doi: 10.1101/lm.251906 , 2006 .

[63]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[64]  E. Koechlin,et al.  Motivation and cognitive control in the human prefrontal cortex , 2009, Nature Neuroscience.

[65]  Alison Adcock,et al.  Enriched encoding: reward motivation organizes cortical networks for hippocampal detection of unexpected events. , 2014, Cerebral cortex.

[66]  James B. Brewer,et al.  Retrieval Search and Strength Evoke Dissociable Brain Activity during Episodic Memory Recall , 2013, Journal of Cognitive Neuroscience.

[67]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[68]  Alison R Preston,et al.  Distributed hippocampal patterns that discriminate reward context are associated with enhanced associative binding. , 2013, Journal of experimental psychology. General.

[69]  E. A. Locke,et al.  Building a practically useful theory of goal setting and task motivation. A 35-year odyssey. , 2002, The American psychologist.

[70]  D. Shohamy,et al.  Intrinsic connectivity between the hippocampus, nucleus accumbens, and ventral tegmental area in humans , 2013, Hippocampus.

[71]  K. Hikosaka,et al.  Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex , 2002, The Journal of Neuroscience.

[72]  R. M. Beckstead Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell-labeling with horseradish peroxidase , 1978, Brain Research.

[73]  H. Arkes Competence and the overjustification effect , 1979 .

[74]  Tara A. Cairo,et al.  Functional connectivity reveals load dependent neural systems underlying encoding and maintenance in verbal working memory , 2006, Neuroscience.

[75]  Mark H. Anshel,et al.  The effect of goal difficulty and task complexity on intrinsic motivation and motor performance. , 1992 .

[76]  Mark D'Esposito,et al.  Influence of Motivation on Control Hierarchy in the Human Frontal Cortex , 2015, The Journal of Neuroscience.

[77]  E. A. Locke,et al.  A theory of goal setting & task performance , 1990 .

[78]  E. Deci,et al.  A meta-analytic review of experiments examining the effects of extrinsic rewards on intrinsic motivation. , 1999, Psychological bulletin.

[79]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[80]  C. Nico Boehler,et al.  Mesolimbic interaction of emotional valence and reward improves memory formation , 2008, Neuropsychologia.

[81]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[82]  Brian Knutson,et al.  Volition to Action—An Event-Related fMRI Study , 2002, NeuroImage.

[83]  Christian Büchel,et al.  Contributions of occipital, parietal and parahippocampal cortex to encoding of object-location associations , 2005, Neuropsychologia.

[84]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[85]  M. Breakspear,et al.  Impact of Load-Related Neural Processes on Feature Binding in Visuospatial Working Memory , 2011, PloS one.