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Necessary, Yet Dissociable Contributions of the Insular and Ventromedial Prefrontal Cortices to Norm Adaptation: Computational and Lesion Evidence in Humans

Xiaosi Gu, Xingchao Wang, Andreas Hula, Shiwei Wang, Shuai Xu, Terry M. Lohrenz, Robert T. Knight, Zhixian Gao, Peter Dayan and P. Read Montague
Journal of Neuroscience 14 January 2015, 35 (2) 467-473; https://doi.org/10.1523/JNEUROSCI.2906-14.2015
Xiaosi Gu
1Wellcome Trust Centre for Neuroimaging, University College London, London, United Kingdom WC1N 3BG,
2Human Neuroimaging Laboratory, Virginia Tech Carilion Research Institute, Roanoke, Virginia 24016,
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Xingchao Wang
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, and
4China National Clinical Research Center for Neurological Diseases, Beijing, China 100050,
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Andreas Hula
1Wellcome Trust Centre for Neuroimaging, University College London, London, United Kingdom WC1N 3BG,
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  • ORCID record for Andreas Hula
Shiwei Wang
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, and
4China National Clinical Research Center for Neurological Diseases, Beijing, China 100050,
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Shuai Xu
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, and
4China National Clinical Research Center for Neurological Diseases, Beijing, China 100050,
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Terry M. Lohrenz
2Human Neuroimaging Laboratory, Virginia Tech Carilion Research Institute, Roanoke, Virginia 24016,
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Robert T. Knight
5Helen Willis Neuroscience Institute and
6Department of Psychology, University of California, Berkeley, California 94720,
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Zhixian Gao
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, and
4China National Clinical Research Center for Neurological Diseases, Beijing, China 100050,
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Peter Dayan
7Gatsby Computational Neuroscience Unit, University College London, London, United Kingdom WC1N 3AR, and
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P. Read Montague
1Wellcome Trust Centre for Neuroimaging, University College London, London, United Kingdom WC1N 3BG,
2Human Neuroimaging Laboratory, Virginia Tech Carilion Research Institute, Roanoke, Virginia 24016,
8Department of Physics, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061
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    Figure 1.

    A, Display of reconstruction of insula lesions (n = 7). B, Display of reconstruction of vmPFC lesions (n = 6). Color bar represents the degree of lesion overlap among patients (0–100%). C, A version of the Ultimatum task. Participants made “accept/reject” responses to an offer of si (of ¥20 Chinese Yuan). D, Time course of one trial. Each participant played 45 rounds in total with a different virtual partner every round.

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    Figure 2.

    A, Rejection rate at each offer size. Patients with vmPFC lesions rejected less in the most unfair conditions (¥ 1 and ¥ 2). B, There were no significant group differences in overall rejection rate. C, The influence of offer size on rejection calculated by a logistic regression model was significantly reduced in patients with vmPFC lesions. D, Trajectories of cumulative rejection rate; *p < 0.05; **p < 0.01; n.s., not significant. L, Left; R, right; B, bilateral. Data are represented as mean ± SEM.

  • Figure 3.
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    Figure 3.

    A, Patients with insula lesions showed slower adaptation rate ε of the RW model with variable initial norm, while patients with vmPFC lesions had higher ε. B, Estimated trajectory of internal norms. C, Patients with insula lesions, but not vmPFC or BDC patients, showed increased sensitivity to norm prediction error α of the RW model. D, Patients with vmPFC lesions, but not insula or BDC patients, showed decreased initial norm of the RW model. E, No significant group difference was detected for the softmax inverse temperature. F, Normalized Bayesian information criterion scores of RW, FS, and Bayes models: the model with the lowest BIC score has the maximal model evidence; *p < 0.05; **p < 0.01; n.s, not significant. L, Left; R, right; B, bilateral. Data are represented as mean ± SEM.

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    Table 1.

    Participant characteristics

    NC (n = 40)BDC (n = 6)Insula (n = 7)vmPFC (n = 6)
    Age (years)*48 ± 1242 ± 1142 ± 854 ± 13
    Sex21 f/19 m2 f/4 m4 f/3 m3 f/3 m
    Handedness39 R/1 L6 R/0 L7 R/0 L6 R/1 L
    Education (years)11 ± 212 ± 313 ± 39 ± 3
    MMSE29 ± 228 ± 228 ± 226 ± 3
    BDI3 ± 43 ± 42 ± 14 ± 4
    Chronicity (months)†—22 ± 1318 ± 2115 ± 2
    Lesion laterality—3 L/3 R4 L/3 R3 L/2 R/1 B
    Lesion size (ml)—42 ± 2032 ± 13112 ± 44
    • L, Left; R, right; B, bilateral; f, female; m, male. MMSE, Mini-Mental Status Exam (Folstein et al., 1975). BDI, Beck Depression Inventory (Knight, 1984). Data are represented as mean ± SD.

    • ↵* The age at the testing date.

    • ↵† The time length between surgery date and testing date.

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The Journal of Neuroscience: 35 (2)
Journal of Neuroscience
Vol. 35, Issue 2
14 Jan 2015
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Necessary, Yet Dissociable Contributions of the Insular and Ventromedial Prefrontal Cortices to Norm Adaptation: Computational and Lesion Evidence in Humans
Xiaosi Gu, Xingchao Wang, Andreas Hula, Shiwei Wang, Shuai Xu, Terry M. Lohrenz, Robert T. Knight, Zhixian Gao, Peter Dayan, P. Read Montague
Journal of Neuroscience 14 January 2015, 35 (2) 467-473; DOI: 10.1523/JNEUROSCI.2906-14.2015

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Necessary, Yet Dissociable Contributions of the Insular and Ventromedial Prefrontal Cortices to Norm Adaptation: Computational and Lesion Evidence in Humans
Xiaosi Gu, Xingchao Wang, Andreas Hula, Shiwei Wang, Shuai Xu, Terry M. Lohrenz, Robert T. Knight, Zhixian Gao, Peter Dayan, P. Read Montague
Journal of Neuroscience 14 January 2015, 35 (2) 467-473; DOI: 10.1523/JNEUROSCI.2906-14.2015
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Keywords

  • brain lesion
  • computational modeling
  • decision-making
  • insular cortex
  • social norms
  • ventromedial prefrontal cortex

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