A functional neuroimaging study of motivation and executive function

Executive functions, such as working memory, must intersect with functions that determine value for the organism. Functional imaging work in humans and single-unit recordings in non-human primates provide evidence that PFC might integrate motivational context with working memory. With functional magnetic resonance imaging (fMRI), we addressed the question of motivation and working memory, using a trial-related design in an object-working memory task. The design permitted the analysis of BOLD signal at separate stages, corresponding to encoding, maintenance, and retrieval. Subjects were motivated by a financial incentive during the task, such that they could gain a high or a low reward. The two different levels of reward also entailed greater or lesser risk of losing money for incorrect responses. In the high, relative to the low, reward condition, subjects shifted response bias, and showed a trend to greater sensitivity. We found main effects in fMRI BOLD signal for reward, which overlapped with BOLD effects for maintenance of information, in the right superior frontal sulcus and bilateral intraparietal sulcus. We also found an interaction between reward and retrieval from working memory in the right dorsolateral prefrontal cortex. Main effects of load and reward occurred in adjacent regions of the ventrolateral PFC during retrieval. The data demonstrate that when subjects perform a simple working memory task, financial incentives motivate performance and interact with some of the same neural networks that process various stages of working memory. Areas of overlap and interaction may integrate information about value, or they may represent a general effect of motivation increasing neural effort.

[1]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[2]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

[3]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[4]  J. Cohen,et al.  Spiral K‐space MR imaging of cortical activation , 1995, Journal of magnetic resonance imaging : JMRI.

[5]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[6]  Masataka Watanabe.  Reward expectancy in primate prefrental neurons , 1996, Nature.

[7]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

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

[9]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

[10]  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.

[11]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[12]  P S Goldman-Rakic,et al.  Spatial working memory deficits in the relatives of schizophrenic patients. , 1995, Archives of general psychiatry.

[13]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[14]  M. Shadlen,et al.  Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque , 1999, Neuron.

[15]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[17]  S. Taylor,et al.  The effect of graded aversive stimuli on limbic and visual activation , 2000, Neuropsychologia.

[18]  P. Goldman-Rakic,et al.  The anatomy of dopamine in monkey and human prefrontal cortex. , 1992, Journal of neural transmission. Supplementum.

[19]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[20]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[21]  Gregor Thut,et al.  Activation of the human brain by monetary reward , 1997, Neuroreport.

[22]  B Macwhinney,et al.  The PsyScope experiment-building system. , 1997, Spatial vision.

[23]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[24]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[25]  T. Robbins,et al.  Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[26]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[27]  Alan C. Evans,et al.  Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Edward Awh,et al.  Spatial versus Object Working Memory: PET Investigations , 1995, Journal of Cognitive Neuroscience.

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

[30]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[31]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[32]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[34]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[35]  P. Goldman-Rakic.  Working memory dysfunction in schizophrenia. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[36]  Thomas Elbert,et al.  Dissociation in human prefrontal cortex of affective influences on working memory-related activity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[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]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

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

[41]  G. Aston-Jones,et al.  Locus coeruleus and regulation of behavioral flexibility and attention. , 2000, Progress in brain research.

[42]  B. Berger,et al.  Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine‐beta‐hydroxylase , 1989, The Journal of comparative neurology.

[43]  Nancy C. Andreasen,et al.  Negative symptoms in schizophrenia , 1982 .

[44]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Jonathan D. Cohen,et al.  Reward and Decision , 2002, Neuron.

[46]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[47]  Karl J. Friston,et al.  Temporal Difference Models and Reward-Related Learning in the Human Brain , 2003, Neuron.

[48]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[49]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[50]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[51]  N C Andreasen,et al.  Negative symptoms in schizophrenia , 1982 .

[52]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[53]  Gregory G. Brown,et al.  Error Rate and Outcome Predictability Affect Neural Activation in Prefrontal Cortex and Anterior Cingulate during Decision-Making , 2002, NeuroImage.

[54]  F ATTNEAVE,et al.  The quantitative study of shape and pattern perception. , 1956, Psychological bulletin.

[55]  P. Niedenthal,et al.  The heart's eye: Emotional influences in perception and attention. , 1994 .

[56]  M. Raichle,et al.  Integration of emotion and cognition in the lateral prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[58]  J. Desmond,et al.  Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory , 1999, NeuroImage.