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Separate neural pathways process different decision costs


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.

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Figure 1: Experimental apparatus.
Figure 2: Delay-based decision making: experiment 1.1.
Figure 3: Representative pictomicrographs of OFC, ACC and sham lesions.
Figure 4: Delay-based decision making: experiment 1.2 and 1.3.
Figure 5: Effort-based decision making.
Figure 6: Spontaneous locomotor activity.


  1. 1

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

    Article  Google Scholar 

  2. 2

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  4. 4

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  15. 15

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  19. 19

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

    CAS  Article  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  29. 29

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

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  37. 37

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

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  41. 41

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

    CAS  Article  Google Scholar 

  42. 42

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

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  Google Scholar 

  50. 50

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

    CAS  Article  Google Scholar 

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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.).

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Corresponding author

Correspondence to Peter H Rudebeck.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

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

Supplementary Fig. 2

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

Supplementary Fig. 3

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

Supplementary Fig. 4

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

Supplementary Fig. 5

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

Supplementary Note (PDF 108 kb)

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Rudebeck, P., Walton, M., Smyth, A. et al. Separate neural pathways process different decision costs. Nat Neurosci 9, 1161–1168 (2006).

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