Article | Published:

Separate neural pathways process different decision costs

Nature Neurosciencevolume 9pages11611168 (2006) | Download Citation



Behavioral ecologists and economists emphasize that potential costs, as well as rewards, influence decision making. Although neuroscientists assume that frontal areas are central to decision making, the evidence is contradictory and the critical region remains unclear. Here it is shown that frontal lobe contributions to cost-benefit decision making can be understood by positing the existence of two independent systems that make decisions about delay and effort costs. Anterior cingulate cortex lesions affected how much effort rats decided to invest for rewards. Orbitofrontal cortical lesions affected how long rats decided to wait for rewards. The pattern of disruption suggested the deficit could be related to impaired associative learning. Impairments of the two systems may underlie apathetic and impulsive choice patterns in neurological and psychiatric illnesses. Although the existence of two systems is not predicted by economic accounts of decision making, our results suggest that delay and effort may exert distinct influences on decision making.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1

    Schultz, W. Behavioral theories and the neurophysiology of reward. Annu. Rev. Psychol. 57, 87–115 (2006).

  2. 2

    Kacelnik, A. & Bateson, M. Risk-sensitivity: crossroads for theories of decision making. Trends Cogn. Sci. 1, 304–309 (1997).

  3. 3

    Bautista, L.M., Tinbergen, J. & Kacelnik, A. To walk or to fly? How birds choose among foraging modes. Proc. Natl. Acad. Sci. USA 98, 1089–1094 (2001).

  4. 4

    Long, A. & Platt, M. Decision making: the virtue of patience in primates. Curr. Biol. 15, R874–R876 (2005).

  5. 5

    Stevens, J.R., Hallinan, E.V. & Hauser, M.D. The ecology and evolution of patience in two New World monkeys. Biol. Lett. 1, 223–226 (2005).

  6. 6

    Stevens, J.R., Rosati, A.G., Ross, K.R. & Hauser, M.D. Will travel for food: spatial discounting in two New World monkeys. Curr. Biol. 15, 1855–1860 (2005).

  7. 7

    Berlin, H.A., Rolls, E.T. & Kischka, U. Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 127, 1108–1126 (2004).

  8. 8

    Bechara, A., Damasio, A.R., Damasio, H. & Anderson, S.W. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15 (1994).

  9. 9

    Winstanley, C.A., Theobald, D.E., Cardinal, R.N. & Robbins, T.W. Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J. Neurosci. 24, 4718–4722 (2004).

  10. 10

    Mobini, S. et al. Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology (Berl.) 160, 290–298 (2002).

  11. 11

    Walton, M.E., Bannerman, D.M., Alterescu, K. & Rushworth, M.F. Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J. Neurosci. 23, 6475–6479 (2003).

  12. 12

    Walton, M.E., Bannerman, D.M. & Rushworth, M.F. The role of rat medial frontal cortex in effort-based decision making. J. Neurosci. 22, 10996–11003 (2002).

  13. 13

    Schweimer, J. & Hauber, W. Involvement of the rat anterior cingulate cortex in control of instrumental responses guided by reward expectancy. Learn. Mem. 12, 334–342 (2005).

  14. 14

    Cardinal, R.N., Pennicott, D.R., Sugathapala, C.L., Robbins, T.W. & Everitt, B.J. Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292, 2499–2501 (2001).

  15. 15

    Cummings, J.L. Frontal-subcortical circuits and human behavior. Arch. Neurol. 50, 873–880 (1993).

  16. 16

    Cousins, M.S. & Salamone, J.D. Nucleus accumbens dopamine depletions in rats affect relative response allocation in a novel cost/benefit procedure. Pharmacol. Biochem. Behav. 49, 85–91 (1994).

  17. 17

    Thiebot, M.H., Le Bihan, C., Soubrie, P. & Simon, P. Benzodiazepines reduce the tolerance to reward delay in rats. Psychopharmacology (Berl.) 86, 147–152 (1985).

  18. 18

    Denk, F. et al. Differential involvement of serotonin and dopamine systems in cost-benefit decisions about delay or effort. Psychopharmacology (Berl.) 179, 587–596 (2005).

  19. 19

    Schoenbaum, G. & Roesch, M. Orbitofrontal cortex, associative learning, and expectancies. Neuron 47, 633–636 (2005).

  20. 20

    Kacelnik, A. in Time and Decision: Economic and Psychological Perspectives on Intertemporal Choice (eds. Loewenstein, G., Read, D. & Baumeister, R.) 115–138 (Russell Sage Foundation, New York, 2003).

  21. 21

    Chudasama, Y. & Robbins, T.W. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J. Neurosci. 23, 8771–8780 (2003).

  22. 22

    Kheramin, S. et al. Role of the orbital prefrontal cortex in choice between delayed and uncertain reinforcers: a quantitative analysis. Behav. Processes 64, 239–250 (2003).

  23. 23

    Cardinal, R.N. Neural systems implicated in delayed and probabilistic reinforcement. Neural Netw. (in the press).

  24. 24

    Kolb, B. Dissociation of the effects of lesions of the orbital or medial aspect of the prefrontal cortex of the rat with respect to activity. Behav. Biol. 10, 329–343 (1974).

  25. 25

    Niv, Y., Daw, N.D. & Dayan, P. in Advances in Neural Information Processing Systems (eds. Weiss, Y., Scholkopf, B. & Platt, J.) 1019–1026 (MIT Press, Cambridge, Massachusetts, 2005).

  26. 26

    Walton, M.E., Kennerley, S.W., Bannerman, D.M., Phillips, P. & Rushworth, M.F. Weighing up the benefits of work: behavioral and neural analyses of effort-related decision making. Neural Netw. (in the press).

  27. 27

    Barbelivien, A., Ruotsalainen, S. & Sirvio, J. Metabolic alterations in the prefrontal and cingulate cortices are related to behavioral deficits in a rodent model of attention-deficit hyperactivity disorder. Cereb. Cortex 11, 1056–1063 (2001).

  28. 28

    Winstanley, C.A., Dalley, J.W., Theobald, D.E. & Robbins, T.W. Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology 29, 1331–1343 (2004).

  29. 29

    Evenden, J.L. Varieties of impulsivity. Psychopharmacology (Berl.) 146, 348–361 (1999).

  30. 30

    Passetti, F., Chudasama, Y. & Robbins, T.W. The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb. Cortex 12, 1254–1268 (2002).

  31. 31

    Roesch, M., Taylor, A.R. & Schoenbaum, G. Encoding of time-discounted rewards in orbitofrontal cortex is independent of value representation. Neuron (in the press).

  32. 32

    Saddoris, M.P., Gallagher, M. & Schoenbaum, G. Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex. Neuron 46, 321–331 (2005).

  33. 33

    Rushworth, M.F., Walton, M.E., Kennerley, S.W. & Bannerman, D.M. Action sets and decisions in the medial frontal cortex. Trends Cogn. Sci. 8, 410–417 (2004).

  34. 34

    Floyd, N.S., Price, J.L., Ferry, A.T., Keay, K.A. & Bandler, R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J. Comp. Neurol. 422, 556–578 (2000).

  35. 35

    Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P. & Busby, S.J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492, 145–177 (2005).

  36. 36

    Burns, S.M. & Wyss, J.M. The involvement of the anterior cingulate cortex in blood pressure control. Brain Res. 340, 71–77 (1985).

  37. 37

    Critchley, H.D. et al. Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126, 2139–2152 (2003).

  38. 38

    Floresco, S.B. & Ghods-Sharifi, S. Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cereb. Cortex published online 22 February 2006 (doi: 10.1093/cercor/bhj143).

  39. 39

    Salamone, J.D., Cousins, M.S. & Bucher, S. Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav. Brain Res. 65, 221–229 (1994).

  40. 40

    Shidara, M., Aigner, T.G. & Richmond, B.J. Neuronal signals in the monkey ventral striatum related to progress through a predictable series of trials. J. Neurosci. 18, 2613–2625 (1998).

  41. 41

    Sugase-Miyamoto, Y. & Richmond, B.J. Neuronal signals in the monkey basolateral amygdala during reward schedules. J. Neurosci. 25, 11071–11083 (2005).

  42. 42

    Shidara, M. & Richmond, B.J. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296, 1709–1711 (2002).

  43. 43

    Salamone, J.D. & Correa, M. Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav. Brain Res. 137, 3–25 (2002).

  44. 44

    Berendse, H.W., Galis-de Graaf, Y. & Groenewegen, H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 316, 314–347 (1992).

  45. 45

    Brog, J.S., Salyapongse, A., Deutch, A.Y. & Zahm, D.S. The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J. Comp. Neurol. 338, 255–278 (1993).

  46. 46

    Tanaka, S.C. et al. Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat. Neurosci. 7, 887–893 (2004).

  47. 47

    Winstanley, C.A., Theobald, D.E., Dalley, J.W., Cardinal, R.N. & Robbins, T.W. Double dissociation between serotonergic and dopaminergic modulation of medial prefrontal and orbitofrontal cortex during a test of impulsive choice. Cereb. Cortex 16, 106–114 (2005).

  48. 48

    Kalenscher, T. et al. Single units in the pigeon brain integrate reward amount and time-to-reward in an impulsive choice task. Curr. Biol. 15, 594–602 (2005).

  49. 49

    Aoki, N., Suzuki, R., Izawa, E., Csillag, A. & Matsushima, T. Localized lesions of ventral striatum, but not arcopallium, enhanced impulsiveness in choices based on anticipated spatial proximity of food rewards in domestic chicks. Behav. Brain Res. 168, 1–12 (2006).

  50. 50

    Bannerman, D.M. et al. Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav. Neurosci. 116, 884–901 (2002).

Download references


We would like to thank G. Daubeny for assistance with histology. This work was supported by the Medical Research Council (P.H.R., M.E.W. and M.F.S.R), the Royal Society (M.F.S.R.) and the Wellcome Trust (M.E.W. and D.M.B.).

Author information


  1. Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford, OX1 3UD, UK

    • Peter H Rudebeck
    • , Mark E Walton
    • , Angharad N Smyth
    • , David M Bannerman
    •  & Matthew F S Rushworth


  1. Search for Peter H Rudebeck in:

  2. Search for Mark E Walton in:

  3. Search for Angharad N Smyth in:

  4. Search for David M Bannerman in:

  5. Search for Matthew F S Rushworth in:

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Peter H Rudebeck.

Supplementary information

  1. Supplementary Fig. 1

    Delay based decision-making training before surgery. (PDF 689 kb)

  2. Supplementary Fig. 2

    Reconstructions of the minimal (left), representative (centre) and maximal (right) OFC lesions in Experiment 1. (PDF 595 kb)

  3. Supplementary Fig. 3

    Reconstructions of the minimal (left), representative (centre) and maximal (right) ACC lesions in Experiment 1. (PDF 805 kb)

  4. Supplementary Fig. 4

    Reconstructions of the minimal (left), representative (centre) and maximal (right) OFC lesions in Experiment 2. (PDF 661 kb)

  5. Supplementary Fig. 5

    Reconstructions of the minimal (left), representative (centre) and maximal (right) ACC lesions in Experiment 2. (PDF 818 kb)

  6. Supplementary Note (PDF 108 kb)

About this article

Publication history




Issue Date


Further reading