Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance

Journal of Comparative Neurology

Volumn 493, Issue 1, 2005, Pages 99-110

  Aston Jones, Gary ^a   Cohen, Jonathan D ^b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Anterior cingulate cortex; Decision making; Neuromodulation; Optimization; Orbitofrontal cortex; Utility

Indexed keywords

AROUSAL; BEHAVIOR; CINGULATE GYRUS; CONFERENCE PAPER; LOCUS CERULEUS; MONKEY; NEUROPHYSIOLOGY; NONHUMAN; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; CEREBRAL CORTEX; COGNITION; DOPAMINE; LEARNING; LOCUS COERULEUS; MOTOR ACTIVITY; NOREPINEPHRINE;

EID: 27844591709     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20723     Document Type: Conference Paper

References (99)

1. Arnsten AF, Steere JC, Hunt RD. 1996. The contribution of alpha 2-noradrenergic mechanisms of prefrontal cortical cognitive function. Potential significance for attention-deficit hyperactivity disorder. Arch Gen Psychiatry 53:448-455.
2. Aston-Jones G. 1985. Behavioral functions of locus coeruleus derived from cellular attributes. Physiol Psych 13:118-126.
3. Aston-Jones G. 2004. Locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G, editor. The rat nervous system, 3rd ed. San Diego: Elsevier Academic Press, p 259-294.
4. Aston-Jones G, Bloom FE. 1981a. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1:876-886.
5. Aston-Jones G, Bloom FE. 1981b. Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1:887-900.
6. Aston-Jones G, Cohen JD. 2005. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403-450.
7. Aston-Jones G, Chiang C, Alexinsky T. 1991. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88:501-520.
8. Aston-Jones G, Rajkowski J, Kubiak P, Alexinsky T. 1994. Locus coeruleus neurons in the monkey are selectively activated by attended stimuli in a vigilance task. J Neurosci 14:4467-4480.
9. Aston-Jones G, Rajkowski J, Kubiak P, Valentino R, Shipley M. 1996. Role of the locus coeruleus in emotional activation. Prog Brain Res 107:379-402.
10. Aston-Jones G, Rajkowski J, Kubiak P. 1997. Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task. Neuroscience 80:697-715.
11. Aston-Jones G, Rajkowski J, Kubiak P, Ivanova S, Usher M, Cohen J. 1998. Neuromodulation and cognitive performance: recent studies of noradrenergic locus coeruleus neurons in behaving monkeys. In: Goldstein D, Eisenhofer G, McCarty R, editors. Catecholamines: bridging basic science with clinical medicine. New York: Academic Press, p 755-759.
12. Aston-Jones G, Rajkowski J, Cohen J. 2000. Locus coeruleus and regulation of behavioral flexibility and attention. Prog Brain Res 126:165-182.
13. Aston-Jones G, Rajkowski J, Lu W, Zhu Y, Cohen JD, Morecraft RJ. 2002. Prominent projections from the orbital prefrontal cortex to the locus coeruleus in monkey. Soc Neurosci Abstr 28:86.89.
14. Barch D, Braver TS, Nystrom LE, Forman SD, Noll DC, Cohen JD. 1997. Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35:1373-1380.
15. Baylis LL, Rolls ET, Baylis GC. 1995. Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate. Neuroscience 64:801-812.
16. Berridge CW, Waterhouse BD. 2003. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42:33-84.
17. Botvinick MM, Nystrom L, Fissell K, Carter CS, Cohen JD. 1999. Conflict monitoring vs. selection-for-action in anterior cingulate cortex. Nature 402:179-181.
18. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. 2001. Conflict monitoring and cognitive control. Psychol Rev 108:624-652.
19. Botvinick M, Cohen JD, Carter CS. 2004. Conflict monitoring and anterior cingulate cortex: an update. Trend Cogn Sci 8:539-546.
20. Bouret S, Sara SJ. 2004. Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci 20:791-802.
21. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JMG, Kantor HL, Gastfriend DR, Riorden JP, Mathew RT, Rosen BR, Hyman SE. 1997. Acute effects of cocaine on human brain activity and emotion. Neuron 19:591-611.
22. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P. 2001. Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 30:619-639.
23. Carmichael ST, Price JL. 1995a. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615-641.
24. Carmichael ST, Price JL. 1995b. Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642-664.
25. Carmichael ST, Clugnet MC, Price JL. 1994. Central olfactory connections in the macaque monkey. J Comp Neurol 346:403-434.
26. Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD. 1998. Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747-749.
27. Clayton EC, Rajkowski J, Cohen JD, Aston-Jones G. 2004. Phasic activation of monkey locus coeruleus neurons by simple decisions in a forced choice task. J Neurosci 24:9914-9920.
28. Cohen JD, Aston-Jones G, Gilzenrat MS. 2004. A systems-level perspective on attention and cognitive control: guided activation, adaptive gating, conflict monitoring, and exploitation vs. exploration. In: Posner MI, editor. Cognitive neuroscience of attention. New York: Guilford Press. p 71-90.
29. Critchley HD, Rolls ET. 1996. Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J Neurophysiol 75:1673-1686.
30. Devinsky O, Morrell MJ, Vogt BA. 1995. Contributions of anterior cingulate cortex to behaviour. Brain 118:279-306.
31. Duncan J, Owen AM. 2000. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475-483.
32. Eisenberger N, Lieberman, MD, Williams, KD. 2003. Does rejection hurt? An FMRI study of social exclusion. Science 302:290-292.
33. Falkenstein M, Hohnsbein J, Hoorman J, Blanke L. 1991. Effects of cross-modal divided attention on late ERP components. II. Error processing in choice reaction tasks. Electroenceph Clin Neurophysiol 78:447-455.
34. Foote SL, Freedman R, Oliver AP. 1975. Effects of putative neurotransmitters on neuronal activity in monkey auditory cortex. Brain Res 86:229-242.
35. Foote SL, Aston-Jones G, Bloom FE. 1980. Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc Natl Acad Sci U S A 77:3033-3037.
36. Foote SL, Bloom FE, Aston-Jones G. 1983. Nucleus locus ceruelus: new evidence of anatomical and physiological specificity. Physiol Rev 63:844-914.
37. Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E. 1993. A neural system for error detection and compensation. Psychol Sci 4:385-390.
38. Gold JI, Shadlen MN. 2000. Representation of a perceptual decision in developing oculomotor commands. Nature 404:390-394.
39. Grant SJ, Aston-Jones G, Redmond DEJ. 1988. Responses of primate locus coeruleus neurons to simple and complex sensory stimuli. Brain Res Bull 21:401-410.
40. Gratton G, Coles MGH, Donchin E. 1992. Optimizing the use of information: strategic control of activation and responses. J Exp Psych Gen 4:480-506.
41. Hanes DP, Schall JD. 1996. Neural control of voluntary movement initiation. Science 274:427-430.
42. Hobson JA, McCarley RW, Wyzinski PW. 1975. Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189:55-58.
43. Holroyd CB, Nieuwenhuis S, Yeung N, Cohen JD. 2003. Errors in reward prediction are reflected in the event-related brain potential. Neuroreport 14:2481-2484.
44. Holroyd C, Larsen, JT, Cohen, JD. 2004a. Context dependence of the event-related brain potential associated with reward and punishment. Psychophysiology 41:245-253.
45. Holroyd CB, Nieuwenhuis S, Yeung N, Nystrom L, Mars R, Coles MGH, Cohen JD. 2004b. Dorsal anterior cingulate cortex is sensitive to internal and external sources of error information: a functional magnetic resonance imaging study. Nat Neurosci 7:497-498.
46. Ito S, Stuphorn V, Brown JW, Schall JD. 2003. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302:120-122.
47. Ivanova S, Rajkowski J, Silakov V, Watanabe T, Aston-Jones G. 1997. Local chemomanipulations of locus coeruleus (LC) activity in monkeys alter cortical event-related potentials (ERPs) and task performance. Soc Neurosci Abstr 23:1587.
48. Jodo E, Aston-Jones G. 1997. Activation of locus coeruleus by prefrontal cortex is mediated by excitatory amino acid inputs. Brain Res 768:327-332.
49. Jodo E, Chiang C, Aston-Jones G. 1998. Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neuroscience 83:63-80.
50. Jones AD, Cho RY, Nystrom LE, Cohen JD, Braver TS. 2002. A computational model of anterior cingulate function in speeded response tasks: effects of frequency, sequence, and conflict. Cogn Affect Behav Neurosci 2:300-317.
51. Jouvet M. 1969. Biogenic amines and the states of sleep. Science 163:32-41.
52. Knutson B, Westdorp A, Kaiser E, Hommer D. 2000. fMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 12:20-27.
53. Kubiak P, Rajkowski J, Aston-Jones G. 1992. Behavioral performance and sensory responsiveness of LC neurons in a vigilance task varies with tonic LC discharge rate. Soc Neurosci Abstr 18:538.
54. Laming DRJ. 1968. Information theory of choice-reaction times. New York: Academic Press.
55. Laming DRJ. 1979. Choice reaction performance following an error. Acta Psychol 43:199-224.
56. McClure SM LD, Loewenstein G, Cohen JD. 2004. Separate neural systems value immediate and delayed monetary rewards. Science 306:503-507.
57. Mesulam M-M. 1981. A cortical network for directed attention and unilateral neglect. Ann Neurol 10:309-325.
58. Miltner WHR, Braun CH, Coles MGH. 1997. Event-related potentials following incorrect feedback in a time-estimation task: evidence for a 'generic' neural system for error detection. J Cogn Neurosci 9:788-798.
59. Morecraft RJ, Geula C, Mesulam MM. 1992. Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J Comp Neurol 323:341-358.
60. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ. 2002. Neural responses during anticipation of a primary taste reward. Neuron 33:815-826.
61. Ongur D, Price JL. 2000. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206-219.
62. Paxinos G, Huang X-F, Toga AW. 2000. The rhesus monkey brain in stereotaxic coordinates. San Diego: Academic Press.
63. Rabbitt PMAJoEP. 1966. Errors and error-correction in choice-response tasks. J Exp Psychol 71:264-272.
64. Rajkowski J, Kubiak P, Ivanova S, Aston-Jones G. 1998. State related activity and reactivity of locus coeruleus neurons in behaving monkeys. In: Goldstein D, Eisenhofer G, McCarty R, editors. Catecholamines: bridging basic science with clinical medicine. New York: Academic Press, p 740-744.
65. Rajkowski J, Lu W, Zhu Y, Cohen J, Aston-Jones G. 2000. Prominent projections from the anterior cingulate cortex to the locus coeruleus in rhesus monkey. Soc Neurosci Abstr 26:838.815.
66. Rajkowski J, Majczynski H, Clayton E, Aston-Jones G. 2004. Activation of monkey locus coeruleus neurons varies with difficulty and behavioral performance in a target detection task. J Neurophysiol 92:361-371.
67. Rasmussen K, Morilak DA, Jacobs BL. 1986. Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli. Brain Res 371:324-334.
68. Ratcliff R. 1978. A theory of memory retrieval. Psychol Rev 85:59-108.
69. Reddi B. 2001. Decision making: two stages of neural judgement. Curr Biol 11:R603-R606.
70. Roesch MR, Olson CR. 2004. Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304:307-310.
71. Rogawski MA, Aghajanian GK. 1982. Activation of lateral geniculate neurons by locus coeruleus or dorsal noradrenergic bundle stimulation: selective blockade by the alpha 1-adrenoceptor antagonist prazosin. Brain Res 250:31-39.
72. Rolls ET. 2004. The functions of the orbitofrontal cortex. Brain Cogn 55:11-29.
73. Rolls ET, Sienkiewicz ZJ, Yaxley S. 1989. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci 1:53-60.
74. Rolls ET, Yaxley S, Sienkiewicz ZJ. 1990. Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J Neurophysiol 64:1055-1066.
75. Rolls ET, Critchley HD, Mason R, Wakeman EA. 1996. Orbitofrontal cortex neurons: role in olfactory and visual association learning. J Neurophysiol 75:1970-1981.
76. Sara SJ, Herve-Minvielle A. 1995. Inhibitory influence of frontal cortex on locus coeruleus neurons. Proc Natl Acad Sci U S A 92:6032-6036.
77. Schall JD. 2003. Neural correlates of decision processes: neural and mental chronometry. Curr Opin Neurobiol 13:182-186.
78. Schall JD, Thompson KG. 1999. Neural selection and control of visually guided eye movements. Annu Rev Neurosci 22:241-259.
79. Schultz W, Tremblay L, Hollerman JR. 2000. Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10:272-284.
80. Segal M, Bloom FE. 1976. The action of norepinephrine in the rat hippocampus. IV. The effects of locus coeruleus stimulation on evoked hippocampal unit activity. Brain Res 107:513-525.
81. Servan-Schreiber D, Printz H, Cohen JD. 1990. A network model of catecholamine effects gain signal to noise ratio and behavior. Science 249:892-895.
82. Shadlen MN, Newsome WT. 1996. Motion perception: seeing and deciding. Proc Natl Acad Sci U S A 93:628-633.
83. Shadlen MN, Newsome WT. 2001. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J Neurophysiol 86:1916-1936.
84. Small DM, Zatorre RJ, Dagher A, Evans AC Jones-Gotman M. 2001. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124:1720-1733.
85. Smith PL, Ratcliff R. 2004. Psychology and neurobiology of simple decisions. Trends Neurosci 27:161-168.
86. Sugrue LP, Corrado GS, Newsome WT. 2004. Matching behavior and the representation of value in the parietal cortex. Science 304:1782-1787.
87. Thorpe SJ, Rolls ET, Maddison S. 1983. The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res 49:93-115.
88. Thut G, Schultz W, Roelcke U, Nienhusmeier M, Missimer J, Maguire RP, Leenders KL. 1997. Activation of the human brain by monetary reward. Neuroreport 8:1225-1228.
89. Tremblay L, Schultz W. 1999. Relative reward preference in primate orbitofrontal cortex. Nature 398:704-708.
90. Ullsperger M, von Cramon DY. 2001. Subprocesses of performance monitoring: a dissociation of error processing and response competition revealed by event-related fMRI and ERPs. Neuroimage 14:1387-1401.
91. Usher M, Cohen JD, Servan-Schreiber D, Rajkowski J, Aston-Jones G. 1999. The role of locus coeruleus in the regulation of cognitive performance. Science 283:549-554.
92. Wald A. 1947. Sequential analysis. New York: John Wiley & Sons.
93. Wallis JD, Miller EK. 2003. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18:2069-2081.
94. Waterhouse BD, Woodward DJ. 1980. Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosensory afferent pathways in the rat. Exp Neurol 67:11-34.
95. Waterhouse BD, Moises HC, Woodward DJ. 1980. Noradrenergic modulation of somatosensory cortical neuronal responses to iontophoretically applied putative neurotransmitters. Exp Neurol 69:30-49.
96. Waterhouse BD, Moises HC, Yeh HH, Geller HM, Woodward DJ. 1984. Comparison of norepinephrine- and benzodiazepine-induced augmentation of Purkinje cell responses to gamma-aminobutyric acid (GABA). J Pharmacol Exp Ther 228:257-267.
97. Williams JT, Henderson G, North RA. 1985. Characterization of alpha 2-adrenoceptors which increase potassium conductance in rat locus coeruleus neurones. Neuroscience 14:95-101.
98. Yeung N, Holroyd C, Cohen J. 2005. ERP correlates of feedback and reward processing in the presence and absence of response choice. Cereb Cortex 15:535-544.
99. Zhu Y, Iba M, Rajkowski J, Aston-Jones G. 2004. Projection from the orbitofrontal cortex to the locus coeruleus in monkeys revealed by anterograde tracing. Soc Neurosci Abstr 30:211.213.