Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The short-latency dopamine signal: a role in discovering novel actions?


An influential concept in contemporary computational neuroscience is the reward prediction error hypothesis of phasic dopaminergic function. It maintains that midbrain dopaminergic neurons signal the occurrence of unpredicted reward, which is used in appetitive learning to reinforce existing actions that most often lead to reward. However, the availability of limited afferent sensory processing and the precise timing of dopaminergic signals suggest that they might instead have a central role in identifying which aspects of context and behavioural output are crucial in causing unpredicted events.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: A latency constraint associated with visual input to dopaminergic neurons.
Figure 2: Evidence supporting the SC as the primary source of short-latency visual input to DA neurons in the SNc.
Figure 3: Potentially converging inputs to the dorsal striatum.
Figure 4: The relative timing of proposed inputs to the dorsal striatum could be crucial for determining the source of agency.
Figure 5: Response of dopaminergic neurons to noxious stimuli.
Figure 6: A possible explanation for why the phasic dopaminergic reinforcement signal precedes any motor activity elicited by an unpredicted salient sensory event.


  1. 1

    Thorndike, E. L. Animal Intelligence (Macmillan, New York, 1911).

    Google Scholar 

  2. 2

    Schultz, W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1–27 (1998).

    CAS  PubMed  Google Scholar 

  3. 3

    Redgrave, P., Prescott, T. J. & Gurney, K. Is the short latency dopamine response too short to signal reward error? Trends Neurosci. 22, 146–151 (1999).

    CAS  PubMed  Google Scholar 

  4. 4

    Comoli, E. et al. A direct projection from superior colliculus to substantia nigra for detecting salient visual events. Nature Neurosci. 6, 974–980 (2003).

    CAS  PubMed  Google Scholar 

  5. 5

    Dommett, E. et al. How visual stimuli activate dopaminergic neurons at short latency. Science 307, 1476–1479 (2005).

    CAS  PubMed  Google Scholar 

  6. 6

    Montague, P. R., Dayan, P. & Sejnowski, T. J. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 16, 1936–1947 (1996).

    CAS  PubMed  Google Scholar 

  7. 7

    Montague, P. R., Hyman, S. E. & Cohen, J. D. Computational roles for dopamine in behavioural control. Nature 431, 760–767 (2004).

    CAS  Google Scholar 

  8. 8

    Schultz, W. Getting formal with dopamine and reward. Neuron 36, 241–263 (2002).

    CAS  Google Scholar 

  9. 9

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

    Google Scholar 

  10. 10

    Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    CAS  PubMed  Google Scholar 

  11. 11

    Gerfen, C. R. & Wilson, C. J. in Handbook of Chemical Neuroanatomy Vol. 12 (eds Swanson, L. W., Bjorklund, A. & Hokfelt, T.) Part III, 371–468 (Elsevier, Amsterdam, 1996).

    Google Scholar 

  12. 12

    Graybiel, A. M. Neurotransmitter and neuromodulators in the basal ganglia. Trends Neurosci. 13, 244–254 (1990).

    CAS  PubMed  Google Scholar 

  13. 13

    Hiroi, N. et al. Molecular dissection of dopamine receptor signaling. J. Chem. Neuroanat. 23, 237–242 (2002).

    CAS  PubMed  Google Scholar 

  14. 14

    Bergman, H. et al. Physiological aspects of information processing in the basal ganglia of normal and Parkinsonian primates. Trends Neurosci. 21, 32–38 (1998).

    CAS  Google Scholar 

  15. 15

    Radad, K., Gille, G. & Rausch, W. D. Short review on dopamine agonists: insight into clinical and research studies relevant to Parkinson's disease. Pharm. Rep. 57, 701–712 (2005).

    CAS  Google Scholar 

  16. 16

    Wise, R. A. Dopamine, learning and motivation. Nature Rev. Neurosci. 5, 483–494 (2004).

    CAS  Google Scholar 

  17. 17

    Berridge, K. C. & Robinson, T. E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 28, 309–369 (1998).

    CAS  Article  Google Scholar 

  18. 18

    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  PubMed  PubMed Central  Google Scholar 

  19. 19

    Marr, D. Vision: A Computational Approach (Freeman & Co., San Francisco, 1982).

    Google Scholar 

  20. 20

    Gurney, K., Prescott, T. J., Wickens, J. R. & Redgrave, P. Computational models of the basal ganglia: from robots to membranes. Trends Neurosci. 27, 453–459 (2004).

    CAS  PubMed  Google Scholar 

  21. 21

    Waelti, P., Dickinson, A. & Schultz, W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Fiorillo, C. D., Tobler, P. N. & Schultz, W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299, 1898–1902 (2003).

    CAS  Google Scholar 

  23. 23

    Tobler, P. N., Fiorillo, C. D. & Schultz, W. Adaptive coding of reward value by dopamine neurons. Science 307, 1642–1645 (2005).

    CAS  Google Scholar 

  24. 24

    Bayer, H. M. & Glimcher, P. W. Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47, 129–141 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Satoh, T., Nakai, S., Sato, T. & Kimura, M. Correlated coding of motivation and outcome of decision by dopamine neurons. J. Neurosci. 23, 9913–9923 (2003).

    CAS  PubMed  Google Scholar 

  26. 26

    Nakahara, H., Itoh, H., Kawagoe, R., Takikawa, Y. & Hikosaka, O. Dopamine neurons can represent context-dependent prediction error. Neuron 41, 269–280 (2004).

    CAS  Google Scholar 

  27. 27

    Tobler, P. N., Dickinson, A. & Schultz, W. Coding of predicted reward omission by dopamine neurons in a conditioned inhibition paradigm. J. Neurosci. 23, 10402–10410 (2003).

    CAS  PubMed  Google Scholar 

  28. 28

    Ungless, M. A. Dopamine: the salient issue. Trends Neurosci. 27, 702–706 (2004).

    CAS  PubMed  Google Scholar 

  29. 29

    Sugrue, L. P., Corrado, G. S. & Newsome, W. T. Choosing the greater of two goods: neural currencies for valuation and decision making. Nature Rev. Neurosci. 6, 363–375 (2005).

    CAS  Google Scholar 

  30. 30

    Salzman, C. D., Belova, M. A. & Paton, J. J. Beetles, boxes and brain cells: neural mechanisms underlying valuation and learning. Curr. Opin. Neurobiol. 15, 721–729 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Houk, J. C. Agents of the mind. Biol. Cybern. 92, 427–437 (2005).

    PubMed  Google Scholar 

  32. 32

    Suri, R. E. TD models of reward predictive responses in dopamine neurons. Neural Netw. 15, 523–533 (2002).

    PubMed  Google Scholar 

  33. 33

    Bar-Gad, I. & Bergman, H. Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr. Opin. Neurobiol. 11, 689–695 (2001).

    CAS  Google Scholar 

  34. 34

    Frank, M. J. Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J. Cogn. Neurosci. 17, 51–72 (2005).

    PubMed  Google Scholar 

  35. 35

    Daw, N. D., Niv, Y. & Dayan, P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nature Neurosci. 8, 1704–1711 (2005).

    CAS  PubMed  Google Scholar 

  36. 36

    Freeman, A. S. Firing properties of substantia nigra dopaminergic neurons in freely moving rats. Life Sci. 36, 1983–1994 (1985).

    CAS  PubMed  Google Scholar 

  37. 37

    Guarraci, F. A. & Kapp, B. S. An electrophysiological characterization of ventral tegmental area dopaminergic neurons during differential pavlovian fear conditioning in the awake rabbit. Behav. Brain Res. 99, 169–179 (1999).

    CAS  PubMed  Google Scholar 

  38. 38

    Horvitz, J. C., Stewart, T. & Jacobs, B. L. Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res. 759, 251–258 (1997).

    CAS  PubMed  Google Scholar 

  39. 39

    Ljungberg, T., Apicella, P. & Schultz, W. Responses of monkey dopamine neurons during learning of behavioural reactions. J. Neurophysiol. 67, 145–163 (1992).

    CAS  PubMed  Google Scholar 

  40. 40

    Pan, W. X., Schmidt, R., Wickens, J. R. & Hyland, B. I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward- learning network. J. Neurosci. 25, 6235–6242 (2005).

    CAS  PubMed  Google Scholar 

  41. 41

    Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

    CAS  PubMed  Google Scholar 

  42. 42

    Mirenowicz, J. & Schultz, W. Importance of unpredictability for reward responses in primate dopamine neurons. J. Neurophysiol. 72, 1024–1027 (1994).

    CAS  PubMed  Google Scholar 

  43. 43

    Coizet, V., Comoli, E., Westby, G. W. M. & Redgrave, P. Phasic activation of substantia nigra and the ventral tegmental area by chemical stimulation of the superior colliculus: an electrophysiological investigation in the rat. Eur. J. Neurosci. 17, 28–40 (2003).

    PubMed  Google Scholar 

  44. 44

    Overton, P. G., Coizet, V., Dommett, E. J. & Redgrave, P. The parabrachial nucleus is a source of short latency nociceptive input to midbrain dopaminergic neurones in rat. Soc. Neurosci. Abstr. 301.5 (2005).

  45. 45

    Coizet, V., Dommett, E. J., Redgrave, P. & Overton, P. G. Nociceptive responses of midbrain dopaminergic neurones are modulated by the superior colliculus in the rat. Neuroscience 139, 1479–1493 (2006).

    CAS  PubMed  Google Scholar 

  46. 46

    McHaffie, J. G. et al. A direct projection from superior colliculus to substantia nigra pars compacta in the cat. Neuroscience 138, 221–234 (2006).

    CAS  PubMed  Google Scholar 

  47. 47

    Horvitz, J. C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96, 651–656 (2000).

    CAS  PubMed  Google Scholar 

  48. 48

    Takikawa, Y., Kawagoe, R. & Hikosaka, O. A possible role of midbrain dopamine neurons in short- and long-term adaptation of saccades to position-reward mapping. J. Neurophysiol. 92, 2520–2529 (2004).

    PubMed  Google Scholar 

  49. 49

    Jay, M. F. & Sparks, D. L. Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J. Neurophysiol. 57, 22–34 (1987).

    CAS  Google Scholar 

  50. 50

    Hikosaka, O. & Wurtz, R. H. Visual and oculomotor function of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J. Neurophysiol. 49, 1230–1253 (1983).

    CAS  PubMed  Google Scholar 

  51. 51

    Thorpe, S. J. & Fabre-Thorpe, M. Seeking categories in the brain. Science 291, 260–263 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Rousselet, G. A., Thorpe, S. J. & Fabre-Thorpe, M. How parallel is visual processing in the ventral pathway? Trends Cogn. Sci. 8, 363–370 (2004).

    PubMed  Google Scholar 

  53. 53

    Schultz, W. & Romo, R. Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioural reactions. J. Neurophysiol. 63, 607–624 (1990).

    CAS  PubMed  Google Scholar 

  54. 54

    Hikosaka, O., Sakamoto, M. & Usui, S. Functional properties of monkey caudate neurons. II. Visual and auditory responses. J. Neurophysiol. 61, 799–813 (1989).

    CAS  PubMed  Google Scholar 

  55. 55

    Matsumura, M., Kojima, J., Gardiner, T. W. & Hikosaka, O. Visual and oculomotor functions of monkey subthalamic nucleus. J. Neurophysiol. 67, 1615–1632 (1992).

    CAS  PubMed  Google Scholar 

  56. 56

    May, P. J. et al. Projections from the superior colliculus to substantia nigra pars compacta in a primate. Soc. Neurosci. Abstr. 450.2 (2005).

  57. 57

    Katsuta, H. & Isa, T. Release from GABAA receptor-mediated inhibition unmasks interlaminar connection within superior colliculus in anesthetized adult rats. Neurosci. Res. 46, 73–83 (2003).

    CAS  PubMed  Google Scholar 

  58. 58

    Wurtz, R. H. & Albano, J. E. Visual-motor function of the primate superior colliculus. Ann. Rev. Neurosci. 3, 189–226 (1980).

    CAS  PubMed  Google Scholar 

  59. 59

    Sparks, D. L. Translation of sensory signals into commands for control of saccadic eye movements: role of the primate superior colliculus. Physiol. Rev. 66, 118–171 (1986).

    CAS  PubMed  Google Scholar 

  60. 60

    Grantyn, R. in Neuroanatomy of the Oculomotor System (ed. Buttner-Ennever, J. A.) 273–333 (Elsevier, Amsterdam, 1988).

    Google Scholar 

  61. 61

    Stein, B. E. & Meredith, M. A. The Merging of the Senses (MIT Press, Cambridge, Massachusetts, 1993).

    Google Scholar 

  62. 62

    Horn, G. & Hill, R. M. Effect of removing the neocortex on the response to repeated sensory stimulation of neurones in the mid-brain. Nature 211, 754–755 (1966).

    CAS  PubMed  Google Scholar 

  63. 63

    Sprague, J. M., Marchiafava, P. L. & Rixxolatti, G. Unit responses to visual stimuli in the superior colliculus of the unanesthetized, mid-pontine cat. Arch. Ital. Biol. 106, 169–193 (1968).

    CAS  PubMed  Google Scholar 

  64. 64

    Ikeda, T. & Hikosaka, O. Reward-dependent gain and bias of visual responses in primate superior colliculus. Neuron 39, 693–700 (2003).

    CAS  PubMed  Google Scholar 

  65. 65

    Hikosaka, O., Nakamura, K. & Nakahara, H. Basal ganglia orient eyes to reward. J. Neurophysiol. 95, 567–584 (2006).

    PubMed  Google Scholar 

  66. 66

    Sutton, R. S. & Barto, A. G. Reinforcement Learning – an Introduction (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  67. 67

    White, N. M. Reward or reinforcement: what's the difference? Neurosci. Biobehav. Rev. 13, 181–186 (1989).

    CAS  PubMed  Google Scholar 

  68. 68

    McHaffie, J. G., Stanford, T. R., Stein, B. E., Coizet, V. & Redgrave, P. Subcortical loops through the basal ganglia. Trends Neurosci. 28, 401–407 (2005).

    CAS  PubMed  Google Scholar 

  69. 69

    Reynolds, J. N. J., Schulz, J. M. & Wickens, J. R. Visual responsiveness of striatal spiny neurons in anaesthetised rats: an in vivo intracellular study. Proc. Int. Australas. Wint. Conf. Brain Res. Abstr. 6.4, 39 (2005).

    Google Scholar 

  70. 70

    Schultz, W., Apicella, P., Romo, R. & Scarnati, E. in Models of Information Processing in the Basal Ganglia (eds Houk, J. C., Davis, J. L. & Beiser, D. G.) 11–27 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  71. 71

    Apicella, P., Legallet, E. & Trouche, E. Responses of tonically discharging neurons in the monkey striatum to primary rewards delivered during different behavioral states. Exp. Brain Res. 116, 456–466 (1997).

    CAS  PubMed  Google Scholar 

  72. 72

    Samejima, K., Ueda, Y., Doya, K. & Kimura, M. Representation of action-specific reward values in the striatum. Science 310, 1337–1340 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. 73

    Crutcher, M. D. & DeLong, M. R. Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp. Brain Res. 53, 244–258 (1984).

    CAS  PubMed  Google Scholar 

  74. 74

    Bickford, M. E. & Hall, W. C. Collateral projections of predorsal bundle cells of the superior colliculus in the rat. J. Comp. Neurol. 283, 86–106 (1989).

    CAS  PubMed  Google Scholar 

  75. 75

    Levesque, M., Charara, A., Gagnon, S., Parent, A. & Deschenes, M. Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 709, 311–315 (1996).

    CAS  PubMed  Google Scholar 

  76. 76

    Mink, J. W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381–425 (1996).

    CAS  PubMed  Google Scholar 

  77. 77

    Reiner, A., Jiao, Y., DelMar, N., Laverghetta, A. V. & Lei, W. L. Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J. Comp. Neurol. 457, 420–440 (2003).

    PubMed  Google Scholar 

  78. 78

    Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann. Rev. Neurosci. 9, 357–381 (1986).

    CAS  PubMed  Google Scholar 

  79. 79

    Haber, S. N. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26, 317–330 (2003).

    PubMed  PubMed Central  Google Scholar 

  80. 80

    Harting, J. K., Updyke, B. V. & VanLieshout, D. P. The visual-oculomotor striatum of the cat: functional relationship to the superior colliculus. Exp. Brain Res. 136, 138–142 (2001).

    CAS  PubMed  Google Scholar 

  81. 81

    Krout, K. E., Loewy, A. D., Westby, G. W. M. & Redgrave, P. Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 431, 198–216 (2001).

    CAS  PubMed  Google Scholar 

  82. 82

    Krout, K. E., Belzer, R. E. & Loewy, A. D. Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 448, 53–101 (2002).

    PubMed  Google Scholar 

  83. 83

    Van der Werf, Y. D., Witter, M. P. & Groenewegen, H. J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Rev. 39, 107–140 (2002).

    PubMed  Google Scholar 

  84. 84

    Smith, Y., Raju, D. V., Pare, J. F. & Sidibe, M. The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 27, 520–527 (2004).

    CAS  PubMed  Google Scholar 

  85. 85

    Parent, M. & Parent, A. Single-axon tracing and three-dimensional reconstruction of centre median-parafascicular thalamic neurons in primates. J. Comp. Neurol. 481, 127–144 (2005).

    PubMed  Google Scholar 

  86. 86

    Matsumoto, N., Minamimoto, T., Graybiel, A. M. & Kimura, M. Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85, 960–976 (2001).

    CAS  PubMed  Google Scholar 

  87. 87

    Wightman, R. M. & Robinson, D. L. Transient changes in mesolimbic dopamine and their association with 'reward'. J. Neurochem. 82, 721–735 (2002).

    CAS  Google Scholar 

  88. 88

    Roitman, M. F., Stuber, G. D., Phillips, P. E. M., Wightman, R. M. & Carelli, R. M. Dopamine operates as a subsecond modulator of food seeking. J. Neurosci. 24, 1265–1271 (2004).

    CAS  PubMed  Google Scholar 

  89. 89

    Centonze, D., Picconi, B., Gubellini, P., Bernardi, G. & Calabresi, P. Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur. J. Neurosci. 13, 1071–1077 (2001).

    CAS  PubMed  Google Scholar 

  90. 90

    Reynolds, J. N. & Wickens, J. R. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw. 15, 507–521 (2002).

    PubMed  Google Scholar 

  91. 91

    Wickens, J. A Theory of the Striatum (Pergamon, Oxford, 1993).

    Google Scholar 

  92. 92

    Hikosaka, O. in The Basal ganglia IV: New Ideas and Data on Structure and Function (eds Percheron, G., McKenzie, J. S. & Feger, J.) 589–596 (Plenum, New York, 1994).

    Google Scholar 

  93. 93

    Redgrave, P., Prescott, T. & Gurney, K. N. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89, 1009–1023 (1999).

    CAS  PubMed  Google Scholar 

  94. 94

    Gurney, K., Prescott, T. J. & Redgrave, P. A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol. Cybern. 84, 401–410 (2001).

    CAS  PubMed  Google Scholar 

  95. 95

    Gurney, K., Prescott, T. J. & Redgrave, P. A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour. Biol. Cybern. 84, 411–423 (2001).

    CAS  PubMed  Google Scholar 

  96. 96

    Prescott, T. J., Gonzalez, F. M. M., Gurney, K., Humphries, M. D. & Redgrave, P. A robot model of the basal ganglia: behavior and intrinsic processing. Neural Netw. 19, 31–61 (2006).

    PubMed  Google Scholar 

  97. 97

    Devenport, L. D. & Holloway, F. A. The rat's resistance to superstition: role of the hippocampus. J. Comp. Physiol. Psychol. 94, 691–705 (1980).

    CAS  PubMed  Google Scholar 

  98. 98

    Roberts, S. & Gharib, A. Variation of bar-press duration: where do new responses come from? Behav. Processes 72, 215–223 (2006).

    PubMed  Google Scholar 

  99. 99

    Wickens, J. R., Reynolds, J. N. J. & Hyland, B. I. Neural mechanisms of reward-related motor learning. Curr. Opin. Neurobiol. 13, 685–690 (2003).

    CAS  PubMed  Google Scholar 

  100. 100

    Paton, J. J., Belova, M. A., Morrison, S. E. & Salzman, C. D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865–870 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 101

    Lisman, J. E. & Grace, A. A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46, 703–713 (2005).

    CAS  PubMed  Google Scholar 

  102. 102

    Schultz, W. Multiple reward signals in the brain. Nature Rev. Neurosci. 1, 199–207 (2000).

    CAS  Google Scholar 

  103. 103

    Schoenbaum, G., Setlow, B., Saddoris, M. P. & Gallagher, M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39, 855–867 (2003).

    CAS  PubMed  Google Scholar 

  104. 104

    Corbit, L. H., Ostlund, S. B. & Balleine, B. W. Sensitivity to instrumental contingency degradation is mediated by the entorhinal cortex and its efferents via the dorsal hippocampus. J. Neurosci. 22, 10976–10984 (2002).

    CAS  PubMed  Google Scholar 

  105. 105

    Corbit, L. H. & Balleine, B. W. The role of prelimbic cortex in instrumental conditioning. Behav. Brain Res. 146, 145–157 (2003).

    PubMed  Google Scholar 

  106. 106

    Padoa-Schioppa, C. & Assad, J. A. Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. 107

    Ungless, M. A., Magill, P. J. & Bolam, J. P. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303, 2040–2042 (2004).

    CAS  Google Scholar 

  108. 108

    Klop, E. M., Mouton, L. J., Hulsebosch, R., Boers, J. & Holstege, G. In cat four times as many lamina I neurons project to the parabrachial nuclei and twice as many to the periaqueductal gray as to the thalamus. Neuroscience 134, 189–197 (2005).

    CAS  PubMed  Google Scholar 

  109. 109

    Dean, P., Redgrave, P. & Westby, G. W. M. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137–147 (1989).

    CAS  PubMed  Google Scholar 

  110. 110

    Dickinson, A. The 28th Bartlett Memorial Lecture. Causal learning: an associative analysis. Q. J. Exp. Psychol. B 54, 3–25 (2001).

    CAS  PubMed  Google Scholar 

  111. 111

    Elsner, B. & Hommel, B. Contiguity and contingency in action-effect learning. Psychol. Res. 68, 138–154 (2004).

    PubMed  Google Scholar 

  112. 112

    Yin, H. H., Knowlton, B. J. & Balleine, B. W. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur. J. Neurosci. 22, 505–512 (2005).

    PubMed  Google Scholar 

  113. 113

    Burgdorf, J. & Panksepp, J. The neurobiology of positive emotions. Neurosci. Biobehav. Rev. 30, 173–187 (2006).

    PubMed  Google Scholar 

  114. 114

    Roesch, M. R. & Olson, C. R. Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304, 307–310 (2004).

    CAS  Google Scholar 

  115. 115

    McDonald, A. J. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44, 15–33 (1991).

    CAS  PubMed  Google Scholar 

  116. 116

    Fudge, J. L., Kunishio, K., Walsh, P., Richard, C. & Haber, S. N. Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience 110, 257–275 (2002).

    CAS  PubMed  Google Scholar 

  117. 117

    Singh, S., Barto, A. G. & Chentanez, N. in Advances in Neural Information Processing Systems 17 (eds Saul, L. K., Weiss, H. & Bottou, L.) 1281–1288 (MIT Press, Cambridge, Massachusetts, 2005).

    Google Scholar 

  118. 118

    Robbins, T. W. & Sahakian, B. J. in Metabolic Disorders of the Nervous System (ed. Rose, F. C.) 244–291 (Pitman, London, 1981).

    Google Scholar 

  119. 119

    Saka, E., Goodrich, C., Harlan, P., Madras, B. K. & Graybiel, A. M. Repetitive behaviors in monkeys are linked to specific striatal activation patterns. J. Neurosci. 24, 7557–7565 (2004).

    CAS  PubMed  Google Scholar 

  120. 120

    Daprati, E. et al. Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition 65, 71–86 (1997).

    CAS  PubMed  Google Scholar 

  121. 121

    Spence, S. A. et al. A PET study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). Brain 120, 1997–2011 (1997).

    Google Scholar 

  122. 122

    Kapur, S., Mizrahi, R. & Li, M. From dopamine to salience to psychosis — linking biology, pharmacology and phenomenology of psychosis. Schiz. Res. 79, 59–68 (2005).

    Google Scholar 

  123. 123

    Wise, S. P., Murray, E. A. & Gerfen, C. R. The frontal-cortex-basal ganglia system in primates. Crit. Rev. Neurobiol. 10, 317–356 (1996).

    CAS  PubMed  Google Scholar 

  124. 124

    Reed, P., Mitchell, C. & Nokes, T. Intrinsic reinforcing properties of putatively neutral stimuli in an instrumental two-level discrimination task. Anim. Learn. Behav. 24, 38–45 (1996).

    Google Scholar 

  125. 125

    St Clair-Smith, R. & MacLaren, D. Response preconditioning effects. J. Exp. Psychol Anim. Behav. Process. 9, 41–48 (1983).

    Google Scholar 

Download references


This work has been supported by the Wellcome Trust (P.R.) and the Engineering and Physical Sciences Research Council (K.G. and P.R.). For their helpful discussions and/or comments on early drafts of the manuscript the authors would like to acknowledge J. Berke, J. Reynolds, A. Seth, E. Salinas, T. Stanford, J. McHaffie, T. Prescott, P. Overton and T. Dickinson.

Author information



Corresponding author

Correspondence to Peter Redgrave.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links


Redgrave's laboratory

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Redgrave, P., Gurney, K. The short-latency dopamine signal: a role in discovering novel actions?. Nat Rev Neurosci 7, 967–975 (2006).

Download citation

Further reading


Quick links

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