Value-based modulation of memory encoding involves strategic engagement of fronto-temporal semantic processing regions

  • Michael S. CohenEmail author
  • Jesse Rissman
  • Nanthia A. Suthana
  • Alan D. Castel
  • Barbara J. Knowlton


A number of prior fMRI studies have focused on the ways in which the midbrain dopaminergic reward system coactivates with hippocampus to potentiate memory for valuable items. However, another means by which people could selectively remember more valuable to-be-remembered items is to be selective in their use of effective but effortful encoding strategies. To broadly examine the neural mechanisms of value on subsequent memory, we used fMRI to assess how differences in brain activity at encoding as a function of value relate to subsequent free recall for words. Each word was preceded by an arbitrarily assigned point value, and participants went through multiple study–test cycles with feedback on their point total at the end of each list, allowing for sculpting of cognitive strategies. We examined the correlation between value-related modulation of brain activity and participants’ selectivity index, which measures how close participants were to their optimal point total, given the number of items recalled. Greater selectivity scores were associated with greater differences in the activation of semantic processing regions, including left inferior frontal gyrus and left posterior lateral temporal cortex, during the encoding of high-value words relative to low-value words. Although we also observed value-related modulation within midbrain and ventral striatal reward regions, our fronto-temporal findings suggest that strategic engagement of deep semantic processing may be an important mechanism for selectively encoding valuable items.


Value Memory Selective encoding Reward Metacognitive control fMRI 


Author note

Funding was provided by NSF Grant No. BCS-0848246 to B.J.K., and by a grant from the Scientific Research Network for Decision Neuroscience and Aging (SRNDNA) (subaward under NIH Grant No. AG039350) to B.J.K., M.S.C., J.R., and A.D.C. We thank Susan Bookheimer, Martin Monti, Gregory Samanez-Larkin, Michael Vendetti, and Aimee Drolet Rossi for helpful suggestions related to the design and analysis of this study. We thank Brian Knutson and Gregory Samanez-Larkin for providing scripts to run the MID task, and Vishnu Murty for providing an anatomical VTA atlas. We also thank Shruti Ullas for assistance with running participants. Portions of this work were presented at the 20th Annual Meeting of the Cognitive Neuroscience Society, San Francisco, CA, and at the Mechanisms of Motivation, Cognition, and Aging Interactions (MoMCAI) conference, Washington, DC.

Supplementary material

13415_2014_275_MOESM1_ESM.doc (195 kb)
ESM 1 (DOC 194 kb)


  1. Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J. D. E. (2006). Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron, 50, 507–517.CrossRefPubMedGoogle Scholar
  2. Ariel, R., & Castel, A. D. (2014). Eyes wide open: Enhanced pupil dilation when selectively studying important information. Experimental Brain Research, 232, 337–344.CrossRefPubMedGoogle Scholar
  3. Badre, D., Poldrack, R. A., Paré-Blagoev, E. J., Insler, R., & Wagner, A. D. (2005). Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron, 47, 907–918.CrossRefPubMedGoogle Scholar
  4. Badre, D., & Wagner, A. D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45, 2883–2901.CrossRefPubMedGoogle Scholar
  5. Bookheimer, S. Y. (2002). Functional MRI of language: New approaches to understanding the cortical organization of semantic processing. Annual Review of Neuroscience, 25, 151–188.CrossRefPubMedGoogle Scholar
  6. Brodmann, K. (1909). Vegleichende Lokalisationslehre der Grosshirnde. Leipzig, Germany: Barth.Google Scholar
  7. Castel, A. D. (2008). The adaptive and strategic use of memory by older adults: Evaluative processing and value-directed remembering. In A. S. Benjamin & B. H. Ross (Eds.), The psychology of learning and motivation (Vol. 48, pp. 225–270). San Diego, CA: Academic Press.Google Scholar
  8. Castel, A. D., Balota, D. A., & McCabe, D. P. (2009). Memory efficiency and the strategic control of attention at encoding: Impairments of value-directed remembering in Alzheimer’s disease. Neuropsychology, 23, 297–306.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Castel, A. D., Benjamin, A. S., Craik, F. I. M., & Watkins, M. J. (2002). The effects of aging on selectivity and control in short-term recall. Memory & Cognition, 30, 1078–1085.CrossRefGoogle Scholar
  10. Castel, A. D., Farb, N. A. S., & Craik, F. I. M. (2007). Memory for general and specific value information in younger and older adults: Measuring the limits of strategic control. Memory & Cognition, 35, 689–700.CrossRefGoogle Scholar
  11. Castel, A. D., Humphries, K. L., Lee, S. S., Galvan, A., Balota, D. A., & McCabe, D. P. (2011). The development of memory efficiency and value-directed remembering across the life span: A cross-sectional study of memory and selectivity. Developmental Psychology, 47, 1553–1564.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Castel, A. D., McGillivray, S., & Friedman, M. C. (2012). Metamemory and memory efficiency in older adults: Learning about the benefits of priority processing and value-directed remembering. In M. Naveh-Benjamin & N. Ohta (Eds.), Memory and aging: Current issues and future directions (pp. 245–270). New York, NY: Psychology Press.Google Scholar
  13. Castel, A. D., Murayama, K., Friedman, M. C., McGillivray, S., & Link, I. (2013). Selecting valuable information to remember: Age-related differences and similarities in self-regulated learning. Psychology and Aging, 28, 232–242.CrossRefPubMedGoogle Scholar
  14. Conway, A. R. A., Kane, M. J., Bunting, M. F., Hambrick, D. Z., Wilhelm, O., & Engle, R. W. (2005). Working memory span tasks: A methodological review and user’s guide. Psychonomic Bulletin & Review, 12, 769–786.CrossRefGoogle Scholar
  15. Costafreda, S. G., Fu, C. H. Y., Lee, L., Everitt, B., Brammer, M. J., & David, A. S. (2006). A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus. Human Brain Mapping, 27, 799–810.CrossRefPubMedGoogle Scholar
  16. Craik, F. I. M., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11, 671–684.CrossRefGoogle Scholar
  17. Craik, F. I. M., & Tulving, E. (1975). Depth of processing and the retention of words in episodic memory. Journal of Experimental Psychology: General, 104, 268–294.CrossRefGoogle Scholar
  18. Frey, U., Matthies, H., Reymann, K. G., & Matthies, H. (1991). The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neuroscience Letters, 129, 111–114.CrossRefPubMedGoogle Scholar
  19. Frey, U., Schroeder, H., & Matthies, H. (1990). Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Research, 522, 69–75.CrossRefPubMedGoogle Scholar
  20. Hanten, G., Li, X., Chapman, S. B., Swank, P., Gamino, J. F., Roberson, G., & Levin, H. S. (2007). Development of verbal selective learning. Developmental Neuropsychology, 32, 585–596.CrossRefPubMedGoogle Scholar
  21. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.Google Scholar
  22. Huang, Y. Y., & Kandel, E. R. (1995). D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proceedings of the National Academy of Sciences, 92, 2446–2450.CrossRefGoogle Scholar
  23. Jay, T. M. (2003). Dopamine: A potential substrate for synaptic plasticity and memory mechanisms. Progress in Neurobiology, 69, 375–390.CrossRefPubMedGoogle Scholar
  24. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841.CrossRefPubMedGoogle Scholar
  25. Kane, M. J., Hambrick, D. Z., Tuholski, S. W., Wilhelm, O., Payne, T. W., & Engle, R. W. (2004). The generality of working memory capacity: A latent variable approach to verbal and visuospatial memory span and reasoning. Journal of Experimental Psychology: General, 133, 189–217.CrossRefGoogle Scholar
  26. Kapur, S., Craik, F. I. M., Tulving, E., Wilson, A. A., Houle, S., & Brown, G. M. (1994). Neuroanatomical correlates of encoding in episodic memory: Levels of processing effect. Proceedings of the National Academy of Sciences, 91, 2008–2011.CrossRefGoogle Scholar
  27. Kim, H. (2011). Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. NeuroImage, 54, 2446–2461.CrossRefPubMedGoogle Scholar
  28. Kirby, K. N., Petry, N. M., & Bickel, W. K. (1999). Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. Journal of Experimental Psychology: General, 128, 78–87.CrossRefGoogle Scholar
  29. Kirchhoff, B. A., & Buckner, R. L. (2006). Functional–anatomic correlates of individual differences in memory. Neuron, 51, 263–274.CrossRefPubMedGoogle Scholar
  30. Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21, RC159.PubMedGoogle Scholar
  31. Lancaster, J. L., Tordesillas-Gutiérrez, D., Martinez, M., Salinas, F., Evans., A., Zilles, K., . . . Fox, P. T. (2007). Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Human Brain Mapping, 28, 1194–1205.Google Scholar
  32. Limbrick-Oldfield, E. H., Brooks, J. C. W., Wise, R. J. S., Padormo, F., Hajnal, J. V., Beckmann, C. F., & Ungless, M. A. (2012). Identification and characterisation of midbrain nuclei using optimised functional magnetic resonance imaging. NeuroImage, 59, 1230–1238.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lisman, J. E., & Grace, A. A. (2005). The hippocampal–VTA loop: Controlling the entry of information into long-term memory. Neuron, 46, 703–713.CrossRefPubMedGoogle Scholar
  34. Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neuroscience & Biobehavioral Reviews, 35, 1219–1236.CrossRefGoogle Scholar
  35. Loftus, G. R., & Wickens, T. D. (1970). Effect of incentive on storage and retrieval processes. Journal of Experimental Psychology: General, 85, 141–147.CrossRefGoogle Scholar
  36. McGillivray, S., & Castel, A. D. (2011). Betting on memory leads to metacognitive improvement in younger and older adults. Psychology and Aging, 26, 137–142.CrossRefPubMedGoogle Scholar
  37. Miotto, E. C., Savage, C. R., Evans, J. J., Wilson, B. A., Martins, M. G., Iaki, S., & Amaro, E., Jr. (2006). Bilateral activation of the prefrontal cortex after strategic semantic cognitive training. Human Brain Mapping, 27, 288–295.CrossRefPubMedGoogle Scholar
  38. Murayama, K., & Kuhbandner, C. (2011). Money enhances memory consolidation—but only for boring material. Cognition, 119, 120–124.CrossRefPubMedGoogle Scholar
  39. Murty, V. P., & Adcock, R. A. (2014). Enriched encoding: Reward motivation organizes cortical networks for hippocampal detection of unexpected events. Cerebral Cortex. doi: 10.1093/cercor/bht063 PubMedGoogle Scholar
  40. Murty, V. P., LaBar, K. S., & Adcock, R. A. (2012). Threat of punishment motivates memory encoding via amygdala, not midbrain, interactions with the medial temporal lobe. Journal of Neuroscience, 32, 8969–8976.CrossRefPubMedPubMedCentralGoogle Scholar
  41. O’Carroll, C. M., Martin, S. J., Sandin, J., Frenguelli, B., & Morris, R. G. M. (2006). Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learning and Memory, 13, 760–769.CrossRefPubMedPubMedCentralGoogle Scholar
  42. O’Doherty, J. P. (2013). Functional contributions of the ventromedial prefrontal cortex in value-based decision making. In D. T. Stuss & R. T. Knight (Eds.), Principles of frontal lobe function (pp. 302–315). New York, NY: Oxford University Press.Google Scholar
  43. Rosen, V. M., & Engle, R. W. (1997). The role of working memory capacity in retrieval. Journal of Experimental Psychology: General, 126, 211–227.CrossRefGoogle Scholar
  44. Samanez-Larkin, G. R., Gibbs, S. E. B., Khanna, K., Nielsen, L., Carstensen, L. L., & Knutson, B. (2007). Anticipation of monetary gain but not loss in healthy older adults. Nature Neuroscience, 10, 787–791.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Savage, C. R., Deckersbach, T., Heckers, S., Wagner, A. D., Schacter, D. L., Alpert, N. M., & Rauch, S. L. (2001). Prefrontal regions supporting spontaneous and directed application of verbal learning strategies: Evidence from PET. Brain, 124, 219–231.CrossRefPubMedGoogle Scholar
  46. Shermohammed, M., Murty, V. P., Smith, D. V., Carter, R. M., Huettel, S., & Adcock, R. A. (2012). Resting-state analysis of the ventral tegmental area and substantia nigra reveals differential connectivity with the prefrontal cortex. Poster presented at the 19th Annual Meeting of the Cognitive Neuroscience Society, Chicago, IL.Google Scholar
  47. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.CrossRefPubMedGoogle Scholar
  48. Soderstrom, N. C., & McCabe, D. P. (2011). The interplay between value and relatedness as bases for metacognitive monitoring and control: Evidence for agenda-based monitoring. Journal of Experimental Psychology: Learning, Memory, and Cognition, 37, 1236–1242.PubMedGoogle Scholar
  49. Spaniol, J., Schain, C., & Bowen, H. J. (2014). Reward-enhanced memory in younger and older adults. Journals of Gerontology. Series B, Psychological and Social Sciences. doi: 10.1093/geronb/gbt044 Google Scholar
  50. Stark, C. E. L., & Squire, L. R. (2001). When zero is not zero: The problem of ambiguous baseline conditions in fMRI. Proceedings of the National Academy of Sciences, 98, 12760–12766.CrossRefGoogle Scholar
  51. Steiger, J. H. (1980). Tests for comparing elements of a correlation matrix. Psychological Bulletin, 87, 245–251.CrossRefGoogle Scholar
  52. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system. An approach to cerebral imaging. Stuttgart, Germany: Thieme.Google Scholar
  53. Thompson-Schill, S. L., D’Esposito, M., Aguirre, G. K., & Farah, M. J. (1997). Role of left prefrontal cortex in retrieval of semantic knowledge: A re-evaluation. Proceedings of the National Academy of Sciences, 94, 14792–14797.CrossRefGoogle Scholar
  54. Toglia, M. P., & Battig, W. F. (1978). Handbook of semantic word norms. Hillsdale, NJ: Erlbaum. Republished online as a supplement to Toglia, M. P. (2009). Withstanding the test of time: The 1978 semantic word norms. Behavior Research Methods, 41, 531–533.Google Scholar
  55. Unsworth, N., Brewer, G. A., & Spillers, G. J. (2013). Working memory capacity and retrieval from long-term memory: The role of controlled search. Memory & Cognition, 41, 242–254.CrossRefGoogle Scholar
  56. Van Essen, D. C., Drury, H. A., Dickson, J., Harwell, J., Hanlon, D., & Anderson, C. H. (2001). An integrated software suite for surface-based analyses of cerebral cortex. Journal of American Medical Informatics Association, 8, 443–459.CrossRefGoogle Scholar
  57. Van Essen, D. C., Glasser, M. F., Dierker, D. L., Harwell, J., & Coalson, T. (2012). Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. Cerebral Cortex, 22, 2241–2262.CrossRefPubMedGoogle Scholar
  58. Wagner, A. D., Paré-Blagoev, E. J., Clark, J., & Poldrack, R. A. (2001). Recovering meaning: Left prefrontal cortex guides controlled semantic retrieval. Neuron, 31, 329–338.CrossRefPubMedGoogle Scholar
  59. Wagner, A. D., Schacter, D. L., Rotte, M., Koutstaal, W., Maril, A., Dale, A. M., . . . Buckner, R. L. (1998). Building memories: Remembering and forgetting of verbal experiences as predicted by brain activity. Science, 288, 1188–1191.CrossRefGoogle Scholar
  60. Watkins, M. J., & Bloom, L. C. (1999). Selectivity in memory: An exploration of willful control over the remembering process. Unpublished manuscript.Google Scholar
  61. Whitney, C., Kirk, K., O’Sullivan, J., Lambon Ralph, M. A., & Jefferies, E. (2011). The neural organization of semantic control: TMS evidence for a distributed network in left inferior frontal and posterior middle temporal gyrus. Cerebral Cortex, 21, 1066–1075.CrossRefPubMedGoogle Scholar
  62. Wolosin, S. M., Zeithamova, D., & Preston, A. R. (2012). Reward modulation of hippocampal subfield activation during successful associative encoding and retrieval. Journal of Cognitive Neuroscience, 24, 1532–1547.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Woolrich, M. W., Ripley, B. D., Brady, J. M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modelling of fMRI data. NeuroImage, 14, 1370–1386.CrossRefPubMedGoogle Scholar
  64. Wu, C. C., Samanez-Larkin, G. R., Katovich, K., & Knutson, B. (2014). Affective traits link to reliable neural markers of incentive anticipation. NeuroImage, 84, 279–289.CrossRefPubMedGoogle Scholar
  65. Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C., & Wager, T. D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8, 665–670.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2014

Authors and Affiliations

  • Michael S. Cohen
    • 1
    Email author
  • Jesse Rissman
    • 1
  • Nanthia A. Suthana
    • 1
  • Alan D. Castel
    • 1
  • Barbara J. Knowlton
    • 1
  1. 1.Department of PsychologyUniversity of CaliforniaLos AngelesUSA

Personalised recommendations