Anticipation of monetary gain but not loss in healthy older adults

A Corrigendum to this article was published on 01 September 2007

This article has been updated

Abstract

Although global declines in structure have been documented in the aging human brain, little is known about the functional integrity of the striatum and prefrontal cortex in older adults during incentive processing. We used event-related functional magnetic resonance imaging to determine whether younger and older adults differed in both self-reported and neural responsiveness to anticipated monetary gains and losses. The present study provides evidence for intact striatal and insular activation during gain anticipation with age, but shows a relative reduction in activation during loss anticipation. These findings suggest that there is an asymmetry in the processing of gains and losses in older adults that may have implications for decision-making.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Age by valence by magnitude interaction in post-task cue ratings.
Figure 2: Between-group t-tests of loss versus nonloss anticipation contrast maps (older adults > younger adults; SVC, z > 2.81; P < 0.005 uncorrected).
Figure 3: BOLD activation extracted from the medial caudate at anticipation.
Figure 4: BOLD activation extracted from the anterior insula at anticipation.

Change history

  • 13 August 2007

    In the version of this article initially published, the first author’s name was incorrect. The first author’s name should be Gregory R Samanez-Larkin. The error has been corrected in the HTML and PDF versions of the article.

Notes

  1. 1.

    *NOTE: In the version of this article initially published, the first author’s name was incorrect. The first author’s name should be Gregory R Samanez-Larkin. The error has been corrected in the HTML and PDF versions of the article.

References

  1. 1

    Park, D.C. & Schwarz, N. (eds.). Cognitive Aging: A Primer (Psychology Press/Taylor & Francis, Philadelphia, 2000).

    Google Scholar 

  2. 2

    Cabeza, R., Nyberg, L. & Park, D. Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging (Oxford University Press, New York, 2005).

    Google Scholar 

  3. 3

    Carstensen, L.L., Mikels, J.A. & Mather, M. Aging and the intersection of cognition, motivation and emotion. in Handbook of the Psychology of Aging (eds. Birren, J.E. & Schaie, K.W.) 343–362 (Academic Press, San Diego, 2005).

    Google Scholar 

  4. 4

    Carstensen, L.L. The influence of a sense of time on human development. Science 312, 1913–1915 (2006).

    CAS  Article  Google Scholar 

  5. 5

    Mather, M. & Carstensen, L.L. Aging and motivated cognition: the positivity effect in attention and memory. Trends Cogn. Sci. 9, 496–502 (2005).

    Article  Google Scholar 

  6. 6

    Knight, M. & Mather, M. The affective neuroscience of aging and its implications for cognition. in The Biological Bases of Personality and Individual Differences (ed. Canli, T.) 159–183 (Guilford Press, New York, 2006).

    Google Scholar 

  7. 7

    Mather, M. et al. Amygdala responses to emotionally valenced stimuli in older and younger adults. Psychol. Sci. 15, 259–263 (2004).

    Article  Google Scholar 

  8. 8

    Marschner, A. et al. Reward-based decision-making and aging. Brain Res. Bull. 67, 382–390 (2005).

    CAS  Article  Google Scholar 

  9. 9

    Backman, L. et al. Age-related cognitive deficits mediated by changes in the striatal dopamine system. Am. J. Psychiatry 157, 635–637 (2000).

    CAS  Article  Google Scholar 

  10. 10

    Kaasinen, V. et al. Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain. Neurobiol. Aging 21, 683–688 (2000).

    CAS  Article  Google Scholar 

  11. 11

    Raz, N. The aging brain observed in vivo: Differential changes and their modifiers. in Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging (eds. Cabeza, R., Nyberg, L. & Park, D.) 19–57 (Oxford University Press, New York, 2005).

    Google Scholar 

  12. 12

    Volkow, N.D. et al. Association between decline in brain dopamine with age and cognitive and motor impairment in healthy individuals. Am. J. Psychiatry 155, 344–349 (1998).

    CAS  Article  Google Scholar 

  13. 13

    Knutson, B., Westdorp, A., Kaiser, E. & Hommer, D. fMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 12, 20–27 (2000).

    CAS  Article  Google Scholar 

  14. 14

    Knutson, B., Adams, C.M., Fong, G.W. & Hommer, D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 21, RC159 (2001).

    CAS  Article  Google Scholar 

  15. 15

    Bjork, J.M. et al. Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J. Neurosci. 24, 1793–1802 (2004).

    CAS  Article  Google Scholar 

  16. 16

    Carstensen, L.L., Pasupathi, M., Mayr, U. & Nesselroade, J.R. Emotional experience in everyday life across the adult life span. J. Pers. Soc. Psychol. 79, 644–655 (2000).

    CAS  Article  Google Scholar 

  17. 17

    Garavan, H., Hester, R., Murphy, K., Fassbender, C. & Kelly, C. Individual differences in the functional neuroanatomy of inhibitory control. Brain Res. 1105, 130–142 (2006).

    CAS  Article  Google Scholar 

  18. 18

    Carstensen, L.L. & Mikels, J.A. At the intersection of emotion and cognition: aging and the positivity effect. Curr. Dir. Psychol. Sci. 14, 117–121 (2005).

    Article  Google Scholar 

  19. 19

    Kisley, M.A., Wood, S. & Burrows, C.L. Looking at the sunny side of life: age-related change in an event-related potential measure of the negativity bias. Psychol. Sci. (in the press).

  20. 20

    Wood, S. & Kisely, M.A. The negativity bias is eliminated in older adults: age related reduction in event related brain potentials associated with evaluative categorization. Psychol. Aging 21, 815–820 (2006).

    Article  Google Scholar 

  21. 21

    Kim, H., Shimojo, S. & O'Doherty, J.P. Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLoS Biol. 4, 1453–1461 (2006).

    CAS  Google Scholar 

  22. 22

    Denburg, N.L., Recknor, E.C., Bechara, A. & Tranel, D. Psychophysiological anticipation of positive outcomes promotes advantageous decision-making in normal older persons. Int. J. Psychophysiol. 61, 19–25 (2006).

    Article  Google Scholar 

  23. 23

    Denburg, N.L., Tranel, D. & Bechara, A. The ability to decide advantageously declines prematurely in some normal older persons. Neuropsychologia 43, 1099–1106 (2005).

    CAS  Article  Google Scholar 

  24. 24

    Knutson, B., Fong, G.W., Bennett, S.M., Adams, C.S. & Hommer, D. A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage 18, 263–272 (2003).

    Article  Google Scholar 

  25. 25

    Knutson, B., Taylor, J., Kaufman, M., Peterson, R. & Glover, G.H. Distributed neural representation of expected value. J. Neurosci. 25, 4806–4812 (2005).

    CAS  Article  Google Scholar 

  26. 26

    Glover, G.H. & Law, C.S. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn. Reson. Med. 46, 515–522 (2001).

    CAS  Article  Google Scholar 

  27. 27

    Cox, R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

    CAS  Article  Google Scholar 

  28. 28

    Neter, J., Kutner, M.H., Nachtsheim, C.J. & Wasserman, W. Applied Linear Statistical Models (Irwin, Chicago, 1996).

    Google Scholar 

  29. 29

    Cohen, M.S. Parametric analysis of fMRI data using linear systems methods. Neuroimage 6, 93–103 (1997).

    CAS  Article  Google Scholar 

  30. 30

    Kuhnen, C.M. & Knutson, B. The neural basis of financial risk-taking. Neuron 47, 763–770 (2005).

    CAS  Article  Google Scholar 

  31. 31

    Gazzaley, A. & D'Esposito, M. BOLD functional MRI and cognitive aging. in Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging (eds. Cabeza, R., Nyberg, L. & Park, D.) 107–131 (Oxford University Press, New York, 2005).

    Google Scholar 

Download references

Acknowledgements

We would like to thank G.E. Wimmer and N.G. Hollon for assistance with data collection. This research was supported by US National Institute on Aging Research Grant AG008816, Center on the Demography and Economics of Health and Aging grant AG017253 and Center on Advancing Decision Making in Aging grant AG024957.

Author information

Affiliations

Authors

Contributions

G.S.L., S.G., L.N., L.C. and B.K. designed the experiment. G.S.L., S.G. and K.K. collected and analyzed the data. All of the authors contributed to the preparation of the manuscript.

Corresponding author

Correspondence to Gregory R Samanez-Larkin.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Post-task cue ratings. (PDF 524 kb)

Supplementary Fig. 2

Gain versus nongain anticipation contrast maps for younger adults and older adults. (PDF 4575 kb)

Supplementary Fig. 3

Loss versus nonloss anticipation contrast maps for younger adults and older adults. (PDF 4429 kb)

Supplementary Fig. 4

BOLD activation extracted from the ventral striatum at anticipation. (PDF 495 kb)

Supplementary Fig. 5

Time courses of activation during anticipation of gain and loss in right ventral striatum. (PDF 654 kb)

Supplementary Fig. 6

Correlations between self-reported affect and brain activation. (PDF 616 kb)

Supplementary Fig. 7

Correlations between self-reported affect and brain activation. (PDF 627 kb)

Supplementary Fig. 8

Time courses of activation during anticipation of gain and loss in left medial caudate. (PDF 651 kb)

Supplementary Fig. 9

Time courses of activation during anticipation of gain and loss in right anterior insula. (PDF 651 kb)

Supplementary Fig. 10

Gain versus nongain outcome contrast maps for younger adults and older adults. (PDF 8582 kb)

Supplementary Fig. 11

Time courses of activation during outcome in left MPFC. (PDF 636 kb)

Supplementary Fig. 12

Time courses of activation during outcome in right ventral striatum. (PDF 639 kb)

Supplementary Fig. 13

MIL task performance. (PDF 582 kb)

Supplementary Fig. 14

MIL task performance over time. (PDF 518 kb)

Supplementary Fig. 15

Time courses of activation from individual participants extracted from voxels in primary visual cortex during a visual localizer task. (PDF 503 kb)

Supplementary Fig. 16

MID task schematic. (PDF 2558 kb)

Supplementary Fig. 17

MIL task schematic. (PDF 1904 kb)

Supplementary Table 1

Group maps for younger adults and older adults. (PDF 64 kb)

Supplementary Table 2

Comparison of older versus younger adults. (PDF 36 kb)

Supplementary Table 3

Monetary incentive learning (MIL) task performance. (PDF 32 kb)

Supplementary Table 4

Demographics, questionnaire data and cognitive test battery results. (PDF 40 kb)

Supplementary Table 5

Placement of 6-mm-diameter VOI spheres. (PDF 45 kb)

Supplementary Discussion

Study 1. (PDF 67 kb)

Supplementary Methods

Study 1. (PDF 103 kb)

Supplementary Results

Study 1. (PDF 143 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Samanez-Larkin, G., Gibbs, S., Khanna, K. et al. Anticipation of monetary gain but not loss in healthy older adults. Nat Neurosci 10, 787–791 (2007). https://doi.org/10.1038/nn1894

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing