The anterior cingulate gyrus signals the net value of others' rewards

Journal of Neuroscience

Volumn 34, Issue 18, 2014, Pages 6190-6200

  Apps, Matthew A J ^a,b,c   Ramnani, Narender ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cingulate; Effort; Empathy; Reward; Social; Value

Indexed keywords

ACCURACY; ADULT; ANTERIOR CINGULATE; ARTICLE; BEHAVIORAL SCIENCE; BOLD SIGNAL; CINGULATE SULCUS; COST BENEFIT ANALYSIS; DECISION MAKING; FACTORIAL DESIGN; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; MALE; NORMAL HUMAN; NUCLEUS ACCUMBENS; PREDICTION; PRIORITY JOURNAL; REACTION TIME; REWARD; SIGNAL DETECTION; SOCIAL INTERACTION; TASK PERFORMANCE; TRAINING; YOUNG ADULT;

CINGULATE; EFFORT; EMPATHY; REWARD; SOCIAL; VALUE;

ADOLESCENT; ADULT; BRAIN MAPPING; CHOICE BEHAVIOR; COST-BENEFIT ANALYSIS; CUES; FACTOR ANALYSIS, STATISTICAL; FEMALE; GYRUS CINGULI; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; JUDGMENT; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; REWARD; YOUNG ADULT;

EID: 84899635598     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2701-13.2014     Document Type: Article

References (78)

1. Alexander WH, Brown JW (2011) Medial prefrontal cortex as an actionoutcome predictor. Nat Neurosci 14:1338-1344. CrossRef Medline
2. Amiez C, Joseph JP, Procyk E (2005) Anterior cingulate error-related activity is modulated by predicted reward. Eur J Neurosci 21:3447-3452. CrossRef Medline
3. Andersson JL, Hutton C, Ashburner J, Turner R, Friston K (2001) Modeling geometric deformations in EPI time series. Neuroimage 13:903-919. CrossRef Medline
4. Apps MA, Balsters JH, Ramnani N (2012) The anterior cingulate cortex: Monitoring the outcomes of others' decisions. Soc Neurosci 7:424-435. CrossRef Medline
5. Apps MA, Green R, Ramnani N (2013a) Reinforcement learning signals in the anterior cingulate cortex code for others' false beliefs. Neuroimage 64:1-9. CrossRef Medline
6. Apps MA, Lockwood PL, Balsters JH (2013b) The role of the midcingulate cortex in monitoring others' decisions. Front Neurosci 7:251. CrossRef Medline
7. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839-851. CrossRef Medline
8. Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL (1999) Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J Comp Neurol 410:343-367. CrossRef Medline
9. Bautista LM, Tinbergen J, Wiersma P, Kacelnik A (1998) Optimal foraging and beyond: how starlings cope with changes in food availability. Am Nat 152:543-561. CrossRef Medline
10. Bautista LM, Tinbergen J, Kacelnik A (2001) To walk or to fly? How birds choose among foraging modes. Proc Natl Acad Sci U S A 98:1089-1094. CrossRef Medline
11. Behrens TE, Hunt LT, Woolrich MW, Rushworth MF (2008) Associative learning of social value. Nature 456:245-249. CrossRef Medline
12. Behrens TE, Hunt LT, Rushworth MF (2009) The computation of social behavior. Science 324:1160-1164. CrossRef Medline
13. Botvinick MM, Huffstetler S, McGuire JT (2009) Effort discounting in human nucleus accumbens. Cogn Affect Behav Neurosci 9:16-27. CrossRef Medline
14. Burke CJ, Brünger C, Kahnt T, Park SQ, Tobler PN (2013) Neural integration of risk and effort costs by the frontal pole: only upon request. J Neurosci 33:1706-+. CrossRef Medline
15. Chang SW, Gariépy JF, Platt ML (2013) Neuronal reference frames for social decisions in primate frontal cortex. Nat Neurosci 16:243-250. CrossRef Medline
16. Charnov EL (1976) Optimal foraging, marginal value theorem. Theor Popul Biol 9:129-136. CrossRef Medline
17. Croxson PL, Walton ME, O'Reilly JX, Behrens TE, Rushworth MF (2009) Effort-based cost-benefit valuation and the human brain. J Neurosci 29: 4531-4541. CrossRef Medline
18. Day JJ, Jones JL, Wightman RM, Carelli RM (2010) Phasic nucleus accumbens dopamine release encodes effort-and delay-related costs. Biological Psychiatry 68:306-309. CrossRef Medline
19. Day JJ, Jones JL, Carelli RM (2011) Nucleus accumbens neurons encode predicted and ongoing reward costs in rats. Eur J Neurosci 33:308-321. CrossRef Medline
20. Deichmann R, Gottfried JA, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19:430-441. CrossRef Medline
21. Floresco SB, Whelan JM (2009) Perturbations in different forms of cost/ benefit decision making induced by repeated amphetamine exposure. Psychopharmacology 205:189-201. CrossRef Medline
22. Floresco SB, Tse MT, Ghods-Sharifi S (2008a) Dopaminergic and glutamatergic regulation of effort-and delay-based decision making. Neuropsychopharmacology 33:1966-1979. CrossRef Medline
23. Floresco SB, St Onge JR, Ghods-Sharifi S, Winstanley CA (2008b) Corticolimbic-striatal circuits subserving different forms of cost-benefit decision making. Cogn Affect Behav Neurosci 8:375-389. CrossRef Medline
24. Font L, Mingote S, Farrar AM, Pereira M, Worden L, Stopper C, Port RG, Salamone JD (2008) Intra-accumbens injections of the adenosine A(2A) agonist CGS 21680 affect effort-related choice behavior in rats. Psychopharmacology 199:515-526. CrossRef Medline
25. Frith CD, Frith U (2006) The neural basis of mentalizing. Neuron 50:531-534. CrossRef Medline
26. Gan JO, Walton ME, Phillips PE (2010) Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine. Nat Neurosci 13:25-27. CrossRef Medline
27. Ghods-Sharifi S, Floresco SB (2010) Differential effects on effort discounting induced by inactivations of the nucleus accumbens core or shell. Behav Neurosci 124:179-191. CrossRef Medline
28. Groenewegen HJ, Berendse HW, Haber SN (1993) organization of the output of the ventral striatopallidal system in the rat-ventral pallidal efferents. Neuroscience 57:113-142. CrossRef Medline
29. Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4-26. CrossRef Medline
30. Hampton AN, Bossaerts P, O'Doherty JP (2008) Neural correlates of mentalizing-related computations during strategic interactions in humans. Proc Natl Acad Sci U S A 105:6741-6746. CrossRef Medline
31. Hauber W, Sommer S (2009) Prefrontostriatal circuitry regulates effortrelated decision making. Cereb Cortex 19:2240-2247. CrossRef Medline
32. Hillman KL, Bilkey DK (2010) Neurons in the rat anterior cingulate cortex dynamically encode cost-benefit in a spatial decision-making task. J Neurosci 30:7705-7713. CrossRef Medline
33. Hillman KL, Bilkey DK (2012) Neural encoding of competitive effort in the anterior cingulate cortex. Nat Neurosci 15:1290-1297. CrossRef Medline
34. Hutton C, Bork A, Josephs O, Deichmann R, Ashburner J, Turner R (2002) Image distortion correction in fMRI: a quantitative evaluation. Neuroimage 16:217-240. CrossRef Medline
35. Jocham G, Neumann J, Klein TA, Danielmeier C, Ullsperger M (2009) Adaptive coding of action values in the human rostral cingulate zone. J Neurosci 29:7489-7496. CrossRef Medline
36. Kagel JH, LevinD (1986) The winners curse and public information in common value auctions. American Economic Review 76:894-920.
37. Kennerley SW, Wallis JD (2009) Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables. Eur J Neurosci 29:2061-2073. CrossRef Medline
38. Kennerley SW, Walton ME, Behrens TE, Buckley MJ, Rushworth MF (2006) Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9:940-947. CrossRef Medline
39. Kennerley SW, Dahmubed AF, Lara AH, Wallis JD (2009) Neurons in the frontal lobe encode the value of multiple decision variables. J Cogn Neurosci 21:1162-1178. CrossRef Medline
40. Kennerley SW, Behrens TE, Wallis JD (2011) Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat Neurosci 14:1581-U1119. CrossRef Medline
41. Knutson B, Bossaerts P (2007) Neural antecedents of financial decisions. J Neurosci 27:8174-8177. CrossRef Medline
42. Kolling N, Behrens TE, Mars RB, Rushworth MF (2012) Neural mechanisms of foraging. Science 336:95-98. CrossRef Medline
43. Kunishio K, Haber SN (1994) Primate cingulostriatal projection-limbic striatal versus sensorimotor striatal input. J Comp Neurol 350:337-356. CrossRef Medline
44. Kurniawan IT, Seymour B, Talmi D, Yoshida W, Chater N, Dolan RJ (2010) Choosing to make an effort: the role of striatum in signaling physical effort of a chosen action. J Neurophysiol 104:313-321. CrossRef Medline
45. Kurniawan IT, Guitart-Masip M, Dayan P, Dolan RJ (2013) Effort and valuation in the brain: the effects of anticipation and execution. J Neurosci 33:6160-6169. CrossRef Medline
46. Lockwood PL, Sebastian CL, McCrory EJ, Hyde ZH, Gu X, De Brito SA, Viding E (2013) Association of callous traits with reduced neural response to others' pain in children with conduct problems. Curr Biol 23:901-905. CrossRef Medline
47. Markowitsch HJ, Emmans D, Irle E, Streicher M, Preilowski B (1985) Cortical and subcortical afferent connections of the primates temporal pole-a study of rhesus-monkeys, squirrel-monkeys, and marmosets. J Comp Neurol 242:425-458. CrossRef Medline
48. Matsumoto M, Matsumoto K, Abe H, Tanaka K (2007) Medial prefrontal cell activity signaling prediction errors of action values. Nat Neurosci 10:647-656. CrossRef Medline
49. Meyniel F, Sergent C, Rigoux L, Daunizeau J, Pessiglione M (2013) Neurocomputational account of how the human brain decides when to have a break. Proc Natl Acad Sci U S A 110:2641-2646. CrossRef Medline
50. Middleton FA, Strick PL (2000) Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. Brain Cogn 42: 183-200. CrossRef Medline
51. Mingote S, Font L, Farrar AM, Vontell R, Worden LT, Stopper CM, Port RG, Sink KS, Bunce JG, Chrobak JJ, Salamone JD (2008) Nucleus accumbens adenosine A(2A) receptors regulate exertion of effort by acting on the ventral striatopallidal pathway. J Neurosci 28:9037-9046. CrossRef Medline
52. Nakano K, Kayahara T, Tsutsumi T, Ushiro H (2000) Neural circuits and functional organization of the striatum. J Neurol 247:V1-V15. CrossRef Medline
53. Nunes EJ, Randall PA, Santerre JL, Given AB, Sager TN, Correa M, Salamone JD (2010) Differential effects of selective adenosine antagonists on the effort-related impairments induced by dopamine d1 and d2 antagonism. Neuroscience 170:268-280. CrossRef Medline
54. Pandya DN, Van HoesenGW, MesulamMM (1981) efferent connections of the cingulate gyrus in the rhesus-monkey. Exp Brain Res 42:319-330. Medline
55. Petrides M, Pandya DN (2007) Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J Neurosci 27:11573-11586. CrossRef Medline
56. Phillips PE, Walton ME, Jhou TC (2007) Calculating utility: preclinical evidence for cost-benefit analysis by mesolimbic dopamine. Psychopharmacology 191:483-495. CrossRef Medline
57. Prévost C, Pessiglione M, Météreau E, Cléry-Melin ML, Dreher JC (2010) Separate valuation subsystems for delay and effort decision costs. J Neurosci 30:14080-14090. CrossRef Medline
58. Quilodran R, Rothé M, Procyk E (2008) Behavioral shifts and action valuation in the anterior cingulate cortex. Neuron 57:314-325. CrossRef Medline
59. Ramnani N, MiallRC (2004) Asystem in the human brain for predicting the actions of others. Nat Neurosci 7:85-90. CrossRef Medline
60. Rescorla RA, Wagner AR (1972) Classical conditioning II: Current research and theory, pp 64-99. New York: Appleton-Century Crofts.
61. Ribas-Fernandes JJ, Solway A, Diuk C, McGuire JT, Barto AG, Niv Y, Botvinick MM (2011) A neural signature of hierarchical reinforcement learning. Neuron 71:370-379. CrossRef Medline
62. Rogers RD, Ramnani N, Mackay C, Wilson JL, Jezzard P, Carter CS, Smith SM (2004) Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition. Biol Psychiatry 55:594-602. CrossRef Medline
63. Rudebeck PH, Buckley MJ, Walton ME, Rushworth MF (2006) A role for the macaque anterior cingulate gyrus in social valuation. Science 313: 1310-1312. CrossRef Medline
64. Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191:461-482. CrossRef Medline
65. Sallet J, Quilodran R, Rothé M, Vezoli J, Joseph JP, Procyk E (2007) Expectations, gains, and losses in the anterior cingulate cortex. Cogn Affect Behav Neurosci 7:327-336. CrossRef Medline
66. Schmidt L, Lebreton M, Clery-Melin M-L, Daunizeau J, Pessiglione M (2012) Neural mechanisms underlying motivation of mental versus physical effort. PLoS Biol 10.
67. Seltzer B, Pandya DN (1989) frontal-lobe connections of the superior temporal sulcus in the rhesus-monkey. J Comp Neurol 281:97-113. CrossRef Medline
68. Silvetti M, Alexander W, Verguts T, Brown J (2013) From conflict management to reward-based decision making: actors and critics in primate medial frontal cortex. Neurosci Biobehav Rev. Advance online publication. Retrieved Nov. 15, 2013. doi:10.1016/j.neubiorev.2013.11.003. CrossRef Medline
69. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan R, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303:1157-1162. CrossRef Medline
70. Spooren WP, Lynd-Balta E, Mitchell S, Haber SN (1996) Ventral pallidostriatal pathway in the monkey: Evidence for modulation of basal ganglia circuits. J Comp Neurol 370:295-312. CrossRef Medline
71. Sutton RS, Barto AG (1998) Reinforcement learning: an introduction. Cambridge, MA: MIT.
72. Vogt BA, PandyaDN (1987) Cingulate cortex of the rhesus monkey. 2. Cortical afferents. J Comp Neurol 262:271-289. CrossRef Medline
73. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR (1995) human cingulate cortexsurface-features, flat maps, and cytoarchitecture. J Comp Neurol 359: 490-506. CrossRef Medline
74. Walton ME, Baudonnat M (2012) The value of competition in the rat race. Nat Neurosci 15:1182-1183. CrossRef Medline
75. Walton ME, Kennerley SW, Bannerman DM, Phillips PE, Rushworth MF (2006) Weighing up the benefits of work: Behavioral and neural analyses of effort-related decision making. Neural Netw 19:1302-1314. CrossRef Medline
76. Walton ME, Groves J, Jennings KA, Croxson PL, Sharp T, Rushworth MF, Bannerman DM (2009) Comparing the role of the anterior cingulate cortex and 6-hydroxydopamine nucleus accumbens lesions on operant effort-based decision making. Eur J Neurosci 29:1678-1691. CrossRef Medline
77. Wanat MJ, Kuhnen CM, Phillips PE (2010) Delays conferred by escalating costs modulate dopamine release to rewards but not their predictors. J Neurosci 30:12020-12027. CrossRef Medline
78. Yoshida K, Saito N, Iriki A, Isoda M (2012) Social error monitoring in macaque frontal cortex. Nat Neurosci 15.