Reward and loss incentives improve spatial working memory by shaping trial-by-trial posterior frontoparietal signals
Youngsun T. Cho,
Flora Moujaes,
Charles H. Schleifer,
Martina Starc,
Jie Lisa Ji,
Nicole Santamauro,
Brendan Adkinson,
Antonija Kolobaric,
Morgan Flynn,
John H. Krystal,
John D. Murray,
Grega Repovs,
Alan Anticevic
Affiliations
Youngsun T. Cho
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA; Yale University, Child Study Center, 230 South Frontage Road, New Haven, CT, 06519, USA; Connecticut Mental Health Center, Clinical Neuroscience Research Unit, 34 Park Street, 3rd floor, New Haven, CT, 06519, USA; Yale University, Interdepartmental Neuroscience Program, Yale University Neuroscience Program, P.O. Box 208074, New Haven, CT, 06520, USA; Corresponding authors.
Flora Moujaes
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Charles H. Schleifer
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Martina Starc
University of Ljubljana, Department of Psychology,
Jie Lisa Ji
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Nicole Santamauro
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Brendan Adkinson
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Antonija Kolobaric
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
Morgan Flynn
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA
John H. Krystal
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA; Yale University, NIAAA Center for Translational Neuroscience of Alcoholism, 34 Park Street, 3rd floor, New Haven, CT 06519 USA
John D. Murray
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA; Yale University, Interdepartmental Neuroscience Program, Yale University Neuroscience Program, P.O. Box 208074, New Haven, CT, 06520, USA; Yale University, Department of Physics, 217 Prospect Street, New Haven, CT, 06511, USA
Grega Repovs
University of Ljubljana, Department of Psychology,
Alan Anticevic
Yale University, Department of Psychiatry, 300 George Street, Suite 901, New Haven, CT, 06511, USA; Connecticut Mental Health Center, Clinical Neuroscience Research Unit, 34 Park Street, 3rd floor, New Haven, CT, 06519, USA; Yale University, Interdepartmental Neuroscience Program, Yale University Neuroscience Program, P.O. Box 208074, New Haven, CT, 06520, USA; University of Zagreb, University Psychiatric Hospital Vrapce; Yale University, Department of Psychology, Box 208205, New Haven, CT, 06520-8205, USA; Yale University, NIAAA Center for Translational Neuroscience of Alcoholism, 34 Park Street, 3rd floor, New Haven, CT 06519 USA; Corresponding authors.
Integrating motivational signals with cognition is critical for goal-directed activities. The mechanisms that link neural changes with motivated working memory continue to be understood. Here, we tested how externally cued and non-cued (internally represented) reward and loss impact spatial working memory precision and neural circuits in human subjects using fMRI. We translated the classic delayed-response spatial working memory paradigm from non-human primate studies to take advantage of a continuous numeric measure of working memory precision, and the wealth of translational neuroscience yielded by these studies. Our results demonstrated that both cued and non-cued reward and loss improved spatial working memory precision. Visual association regions of the posterior prefrontal and parietal cortices, specifically the precentral sulcus (PCS) and intraparietal sulcus (IPS), had increased BOLD signal during incentivized spatial working memory. A subset of these regions had trial-by-trial increases in BOLD signal that were associated with better working memory precision, suggesting that these regions may be critical for linking neural signals with motivated working memory. In contrast, regions straddling executive networks, including areas in the dorsolateral prefrontal cortex, anterior parietal cortex and cerebellum displayed decreased BOLD signal during incentivized working memory. While reward and loss similarly impacted working memory processes, they dissociated during feedback when money won or avoided in loss was given based on working memory performance. During feedback, the trial-by-trial amount and valence of reward/loss received was dissociated amongst regions such as the ventral striatum, habenula and periaqueductal gray. Overall, this work suggests motivated spatial working memory is supported by complex sensory processes, and that the IPS and PCS in the posterior frontoparietal cortices may be key regions for integrating motivational signals with spatial working memory precision.
