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On the relationship between emotion and cognition

Nature Reviews Neuroscience volume 9, pages 148–158 (2008)Cite this article

Abstract

The current view of brain organization supports the notion that there is a considerable degree of functional specialization and that many regions can be conceptualized as either 'affective' or 'cognitive'. Popular examples are the amygdala in the domain of emotion and the lateral prefrontal cortex in the case of cognition. This prevalent view is problematic for a number of reasons. Here, I will argue that complex cognitive–emotional behaviours have their basis in dynamic coalitions of networks of brain areas, none of which should be conceptualized as specifically affective or cognitive. Central to cognitive–emotional interactions are brain areas with a high degree of connectivity, called hubs, which are critical for regulating the flow and integration of information between regions.

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Figure 1: Brain connectivity graph.
Figure 2: Circuit for the processing of visual information.
Figure 3: Circuit for executive control.
Figure 4: Conceptual proposal for the relationship between anatomical sites, neural computations and behaviours.

References

  1. Damasio, A. R. Descartes' error: Emotion, reason, and the human brain (ed. Putnam, G. P. New York, 1994).

    Google Scholar 

  2. Phelps, E. A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 57, 27–53 (2006).

    PubMed  Google Scholar 

  3. Davis, M. & Whalen, P. J. The amygdala: Vigilance and emotion. Molecular Psychology 6, 13–34 (2001).

    CAS  Google Scholar 

  4. Dolan, R. Emotion, cognition, and behavior. Science 298, 1191–1194 (2003).

    Google Scholar 

  5. Davidson, R. J., Pizzagalli, D., Nitschke, J. B. & Kalin, N. H. Parsing the subcomponents of emotion and disorders of emotion: Perspectives from affective neuroscience in Handbook of affective sciences (eds Davidson, R. J., Scherer, K. R. & Goldsmith, H. H.) 8–24 (Oxford University Press, New York, 2003).

    Google Scholar 

  6. Moll, J., Zahn, R., de Oliveira-Souza, R., Krueger, F. & Grafman, J. The neural basis of human moral cognition. Nature Rev. Neurosci. 6, 799–809 (2005).

    CAS  Google Scholar 

  7. Drevets, W. C. & Raichle, M. E. Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: Implications for interactions between emotion and cognition. Cogn. Emot. 12, 353–385 (1998).

    Google Scholar 

  8. Fuster, J. M. & Alexander, G. E. Neuron activity related to short-term memory. Science 173, 652–654 (1971).

    CAS  PubMed  Google Scholar 

  9. Kubota, K. & Niki, H. Prefrontal cortical unit activity and delayed alternation performance in monkeys. J. Neurophysiol. 34, 337–347 (1971).

    CAS  PubMed  Google Scholar 

  10. Rolls, E. T. Emotion explained (Oxford University Press, Oxford, 2005).

    Google Scholar 

  11. Arnold, M. B. Emotion and personality (Columbia University Press, New York, 1960).

    Google Scholar 

  12. Ekman, P. An argument for basic emotions. Cogn. Emot. 6, 169–200 (1992).

    Google Scholar 

  13. Haidt, J. The moral emotions in Handbook of Affective Sciences (eds Davidson, R. J., Scherer, K. R. & Goldsmith, H. H.) 852–870 (Oxford University Press, Oxford, 2003).

    Google Scholar 

  14. Damasio, A. R. The feeling of what happens: body and emotion in the making of consciousness (Harcourt Brace, New York, 1999).

    Google Scholar 

  15. Whalen, P. J., et al. Human amygdala responsivity to masked fearful eye whites. Science 306, 2061 (2004).

    CAS  PubMed  Google Scholar 

  16. Ohman, A. Automaticity and the amygdala: nonconscious responses to emotional faces. Curr. Dir. Psychol. Sci. 11, 62–66 (2002).

    Google Scholar 

  17. Pessoa, L. To what extent are emotional visual stimuli processed without attention and awareness? Curr. Opin. Neurobiol. 15, 188–196 (2005).

    CAS  PubMed  Google Scholar 

  18. Papez, J. W. A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38, 725–743 (1937).

    Google Scholar 

  19. MacLean, P. D. Psychosomatic disease and the 'visceral brain': recent developments bearing on the Papez theory of emotion. Psychosom. Med. 11, 338–353 (1949).

    CAS  PubMed  Google Scholar 

  20. Duncan, S. & Barrett, L. F. Affect is a form of cognition: A neurobiological analysis. Cogn. Emot. 21, 1184–1211 (2007).

    PubMed  PubMed Central  Google Scholar 

  21. Lewis, M. D. & Todd, R. M. The self-regulating brain: Cortical-subcortical feedback and the development of intelligent action. Cogn. Dev. 22, 406–430 (2007).

    Google Scholar 

  22. Whalen, P. J. Fear, vigilance, and ambiguity: Initial neuroimaging studies of the human amygdala. Curr. Dir. Psychol. Sci. 7, 177–188 (1998).

    Google Scholar 

  23. Baxter, M. G. & Murray, E. A. The amygdala and reward. Nature Rev. Neurosci. 3, 563–573 (2002).

    CAS  Google Scholar 

  24. Sander, D., Grafman, J. & Zalla, T. The human amygdala: an evolved system for relevance detection. Nature Rev. Neurosci. 14, 303–316 (2003).

    Google Scholar 

  25. Barrett, L. F. & Wager, T. D. The structure of emotion. Curr. Dir. Psychol. Sci. 15, 79–83 (2006).

    Google Scholar 

  26. Aggleton, J. ed. The amygdala: A functional analysis (Oxford University Press, Oxford, 2000).

    Google Scholar 

  27. Aggleton, J. P. The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (Wiley-Liss, Inc., New York, 1992).

    Google Scholar 

  28. Holland, P. C. & Gallagher, M. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci. 3, 65–73 (1999).

    CAS  PubMed  Google Scholar 

  29. Desimone, R. & Duncan, J. Neural mechanisms of selective attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    CAS  PubMed  Google Scholar 

  30. Kastner, S. & Ungerleider, L. G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 (2000).

    CAS  PubMed  Google Scholar 

  31. Pessoa, L., Kastner, S. & Ungerleider, L. G. Attentional control of the processing of neutral and emotional stimuli. Cogn. Brain Res. 15, 31–45 (2002).

    Google Scholar 

  32. Vuilleumier, P. How brains beware: neural mechanisms of emotional attention. Trends Cogn. Sci. 9, 585–594 (2005).

    PubMed  Google Scholar 

  33. Anderson, A. K. & Phelps, E. A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309 (2001).

    CAS  PubMed  Google Scholar 

  34. Morris, J. S., et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121 (Pt 1), 47–57 (1998).

    PubMed  Google Scholar 

  35. Pessoa, L., McKenna, M., Gutierrez, E. & Ungerleider, L. G. Neural processing of emotional faces requires attention. Proc. Natl Acad. Sci. USA 99, 11458–11463 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J. & Dolan, R. J. Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neurosci. 7, 1271–1278 (2004).

    CAS  PubMed  Google Scholar 

  37. Lim, S. L., Padmala, S. & Pessoa, L. Affective learning modulates spatial competition during low-load attentional conditions. Neuropsychologia (2008).

  38. Lim, S. L. & Pessoa, L. Affective learning increases sensitivity to graded emotional faces. Emotion (2008).

  39. Padmala, S., Lim, S. L. & Pessoa, L. Classical conditioning increases visual detection sensitivity and evoked responses in early retinotopically organized visual cortex in Society for Neuroscience (Society for Neuroscience, San Diego, 2007).

    Google Scholar 

  40. Phelps, E. A. & LeDoux, J. E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187 (2005).

    CAS  PubMed  Google Scholar 

  41. Phelps, E. A., Ling, S. & Carrasco, M. Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychol. Sci. 17, 292–299 (2006).

    PubMed  Google Scholar 

  42. Weinberger, N. M. Retuning the brain by fear conditioning in The Cognitive Neurosciences (ed. Gazzaniga M. S.) 1071–1089 (The MIT Press, Cambridge, MA, 1995).

    Google Scholar 

  43. Armony, J. L. & Dolan, R. J. Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study. Neuropsychologia 40, 817–826 (2002).

    PubMed  Google Scholar 

  44. Vuilleumier, P., Armony, J. L., Driver, J. & Dolan, R. J. Effects of attention and emotion on face processing in the human brain: An event-related fMRI study. Neuron 30, 829–841 (2001).

    CAS  PubMed  Google Scholar 

  45. Pessoa, L., McKenna, M., Gutierrez, E. & Ungerleider, L. G. Neural processing of emotional faces requires attention. Proc. Natl Acad. Sci. USA 99, 11458–11463 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Ishai, A., Pessoa, L., Bikle, P. C. & Ungerleider, L. G. Repetition suppression of faces is modulated by emotion. Proc. Natl Acad. Sci. USA 101, 9827–9832 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Pessoa, L., Padmala, S. & Morland, T. Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28, 249–255 (2005).

    PubMed  Google Scholar 

  48. Pessoa, L. & Padmala, S. Quantitative prediction of perceptual decisions during near-threshold fear detection. Proc. Natl Acad. Sci. USA 102, 5612–5617 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Pessoa, L., Japee, S., Sturman, D. & Ungerleider, L. G. Target visibility and visual awareness modulate amygdala responses to fearful faces. Cereb. Cortex 16, 366–375 (2006).

    PubMed  Google Scholar 

  50. Pessoa, L. & Padmala, S. Decoding near-threshold perception of fear from distributed single-trial brain activation. Cereb. Cortex 17, 691–701 (2007).

    PubMed  Google Scholar 

  51. Hsu, S. M. & Pessoa, L. Dissociable effects of bottom-up and top-down factors on the processing of unattended fearful faces. Neuropsychologia 45, 3075–3086 (2007).

    PubMed  PubMed Central  Google Scholar 

  52. Thielscher, A. & Pessoa, L. Neural correlates of perceptual choice and decision making during fear-disgust discrimination. J. Neurosci. 27, 2908–2917 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Blair, K. S., et al. Modulation of emotion by cognition and cognition by emotion. Neuroimage 35, 430–440 (2007).

    CAS  PubMed  Google Scholar 

  54. Bishop, S. J., Jenkins, R. & Lawrence, A. D. Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. Cereb. Cortex 17, 1595–1603 (2007).

    PubMed  Google Scholar 

  55. Bishop, S. J. Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn. Sci. 11, 307–316 (2007).

    PubMed  Google Scholar 

  56. Silvert, L., et al. Influence of attentional demands on the processing of emotional facial expressions in the amygdala. Neuroimage 38, 357–366 (2007).

    PubMed  Google Scholar 

  57. Bishop, S. J., Duncan, J. & Lawrence, A. D. State anxiety modulation of the amygdala response to unattended threat-related stimuli. J. Neurosci. 24, 10364–10368 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Mitchell, D. G., et al. The impact of processing load on emotion. Neuroimage 34, 1299–1309 (2007).

    CAS  PubMed  Google Scholar 

  59. Ochsner, K. N. & Gross, J. J. The cognitive control of emotion. Trends Cogn. Sci. 9, 242–249 (2005).

    PubMed  Google Scholar 

  60. Fangel, C. & Kaada, B. R. Behavior “attention” and fear induced by cortical stimulation in the cat. Electroencephalogr. Clin. Neurophysiol. 12, 575–588 (1960).

    CAS  PubMed  Google Scholar 

  61. Barbas, H. & Zikopoulos, B. Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex in The orbitofrontal cortex (ed. Zald, D. H. & Rauch, S. L.) 57–91 (Oxford University Press, New York, 2006).

    Google Scholar 

  62. Schaefer, A., et al. Individual differences in amygdala activity predict response speed during working memory. J. Neurosci. 26, 10120–10128 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Schaefer, A. & Gray, J. R. A role for the human amygdala in higher cognition. Rev. Neurosci. 18, 355–364 (2007).

    PubMed  Google Scholar 

  64. Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nature Rev. Neurosci. 3, 201–215 (2002).

    CAS  Google Scholar 

  65. Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    CAS  PubMed  Google Scholar 

  66. Pessoa, L. & Ungerleider, L. G. Top-down mechanisms for working memory and attentional processes in The new cognitive neurosciences, 3rd Edition (ed. Gazzaniga, M. S.) 919–930 (MIT Press, Cambridge, MA, 2004).

    Google Scholar 

  67. Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S. & Cohen, J. D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).

    CAS  PubMed  Google Scholar 

  68. Nauta, W. J. H. The problem of the frontal lobe: a reinterpretation. J. Psychiatr. Res. 8, 167–187 (1971).

    CAS  PubMed  Google Scholar 

  69. Davidson, R. J. & Irwin, W. The functional neuroanatomy of emotion and affective style. Trends Cogn. Sci. 3, 11–21 (1999).

    CAS  PubMed  Google Scholar 

  70. Cohen, J. D. The vulcanization of the human brain: A neural perspective on interactions between cognition and emotion. J. Econ. Perspect. 19, 3–24 (2005).

    Google Scholar 

  71. Pribram, K. H. The new neurology and the biology of emotion: a structural approach. Am. Psychol. 22, 830–838 (1967).

    CAS  PubMed  Google Scholar 

  72. Pribram, K. H. The limbic systems, efferent control of neural inhibition and behavior. Prog. Brain Res. 27, 318–336 (1967).

    CAS  PubMed  Google Scholar 

  73. Bush, G., Luu, P. & Posner, M. I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222 (2000).

    CAS  PubMed  Google Scholar 

  74. Rubia, K., Smith, A. B., Brammer, M. J. & Taylor, E. Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20, 351–358 (2003).

    PubMed  Google Scholar 

  75. Aron, A. R., Robbins, T. W. & Poldrack, R. A. Inhibition and the right inferior frontal cortex. Trends Cogn. Sci. 8, 170–177 (2004).

    PubMed  Google Scholar 

  76. Goldstein, M., et al. Neural substrates of the interaction of emotional stimulus processing and motor inhibitory control: an emotional linguistic go/no-go fMRI study. Neuroimage 36, 1026–1040 (2007).

    PubMed  Google Scholar 

  77. Perlstein, W. M., Elbert, T. & Stenger, V. A. Dissociation in human prefrontal cortex of affective influences on working memory-related activity. Proc. Natl Acad. Sci. USA 99, 1736–1741 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Gray, J. R., Braver, T. S. & Raichle, M. E. Integration of emotion and cognition in the lateral prefrontal cortex. Proc. Natl Acad. Sci. USA 99, 4115–4120 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Erk, S., Kleczar, A. & Walter, H. Valence-specific regulation effects in a working memory task with emotional context. Neuro Image 37, 623–632 (2007).

    PubMed  Google Scholar 

  80. Mitchell, R. L. & Phillips, L. H. The psychological, neurochemical and functional neuroanatomical mediators of the effects of positive and negative mood on executive functions. Neuropsychologia 45, 617–629 (2007).

    PubMed  Google Scholar 

  81. Herrington, J. D., et al. Emotion-modulated performance and activity in left dorsolateral prefrontal cortex. Emotion 5, 200–207 (2005).

    PubMed  Google Scholar 

  82. Heller, W. & Nitschke, J. B. Regional brain activity in emotion: A framework for understanding cognition in depression. Cogn. Emot. 11, 637–661 (1997).

    Google Scholar 

  83. Mesulam, M.-M. Behavioral neuroanatomy: Large-scale networks, association cortex, frontal syndromes, the limbic system, and hemispheric specializations in Principles of behavioral and cognitive neurology (ed. Mesulam, M.) 1–120 (Oxford University Press, New York, 2000).

    Google Scholar 

  84. Sporns, O., Chialvo, D. R., Kaiser, M. & Hilgetag, C. C. Organization, development and function of complex brain networks. Trends Cogn. Sci. 8, 418–425 (2004).

    PubMed  Google Scholar 

  85. Sporns, O. & Zwi, J. D. The small world of the cerebral cortex. Neuroinformatics 2, 145–162 (2004).

    PubMed  Google Scholar 

  86. Sporns, O., Tononi, G. & Edelman, G. M. Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb. Cortex 10, 127–141 (2000).

    CAS  PubMed  Google Scholar 

  87. Hilgetag, C. C., Burns, G. A., O'Neill, M. A., Scannell, J. W. & Young, M. P. Anatomical connectivity defines the organization of clusters of cortical areas in the macaque monkey and the cat. Phil. Trans. R. Soc. Lond. 355, 91–110 (2000).

    CAS  Google Scholar 

  88. Sporns, O. Small-world connectivity, motif composition, and complexity of fractal neuronal connections. Biosystems 85, 55–64 (2006).

    PubMed  Google Scholar 

  89. Young, M. P., Scannell, J. W., Burns, G. A. & Blakemore, C. Analysis of connectivity: Neural systems in the cerebral cortex. Rev. Neurosci. 5, 227–249 (1994).

    CAS  PubMed  Google Scholar 

  90. Stephan, K. E., et al. Computational analysis of functional connectivity between areas of primate cerebral cortex. Phil. Trans. R. Soc. Lond. 355, 111–126 (2000).

    CAS  Google Scholar 

  91. Mesulam, M.-M. The human frontal lobes: Transcending the default mode through contingent encoding. in Principles of frontal lobe function (eds Stuss, D. T. & Knight, R. T.) 8–30 (Oxford University Press, New York, 2002).

    Google Scholar 

  92. LeDoux, J. E. The emotional brain (Simon & Schuster, New York, 1996).

    Google Scholar 

  93. Barbas, H. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci. Biobehav. Rev. 19, 449–510 (1995).

    Google Scholar 

  94. Swanson, L. W. The amygdala and its place in the cerebral hemisphere. Ann. NY Acad. Sci. 985, 174–184 (2003).

    PubMed  Google Scholar 

  95. Risold, P. Y., Thompson, R. H. & Swanson, L. W. The structural organization of connections between hypothalamus and cerebral cortex. Brain Res. Brain Res. Rev. 24, 197–254 (1997).

    CAS  PubMed  Google Scholar 

  96. Swanson, L. W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113–164 (2000).

    CAS  PubMed  Google Scholar 

  97. Swanson, L. W. Brain architecture: Understanding the basic plan (Oxford University Press, New York, 2003).

    Google Scholar 

  98. Heimer, L. & Van Hoesen, G. W. The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci. Biobehav. Rev. 30, 126–147 (2006).

    PubMed  Google Scholar 

  99. Sarter, M. & Bruno, J. P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neurosci. 95, 933–952 (2000).

    CAS  Google Scholar 

  100. Sarter, M. & Bruno, J. P. Abnormal regulation of corticopetal cholinergic neurons and impaired information processing in neuropsychiatric disorders. Trends Neurosci. 22, 67–74 (1999).

    CAS  PubMed  Google Scholar 

  101. Sarter, M., Bruno, J. P. & Turchi, J. Basal forebrain afferent projections modulating cortical acetylcholine, attention, and implications for neuropsychiatric disorders. Ann. NY Acad. Sci. 877, 368–382 (1999).

    CAS  PubMed  Google Scholar 

  102. Zaborszky, L. The modular organization of brain systems. Basal forebrain: the last frontier. Prog. Brain Res. 136, 359–372 (2002).

    PubMed  Google Scholar 

  103. Zaborszky, L., Buhl, D. L., Pobalashingham, S., Bjaalie, J. G. & Nadasdy, Z. Three-dimensional chemoarchitecture of the basal forebrain: spatially specific association of cholinergic and calcium binding protein-containing neurons. Neurosci. 136, 697–713 (2005).

    CAS  Google Scholar 

  104. Zaborszky, L., Pang, K., Somogyi, J., Nadasdy, Z. & Kallo, I. The basal forebrain corticopetal system revisited. Ann. NY Acad. Sci. 877, 339–367 (1999).

    CAS  PubMed  Google Scholar 

  105. Alheid, G. F. & Heimer, L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neurosci. 27, 1–39 (1988).

    CAS  Google Scholar 

  106. Zahm, D. S. The evolving theory of basal forebrain functional-anatomical 'macrosystems'. Neurosci. Biobehav Rev. 30, 148–172 (2006).

    PubMed  Google Scholar 

  107. Amaral, D. G., Price, J. L., Pitkanen, A. & Carmichael, S. T. Anatomical organization of the primate amygdaloid complex in The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (ed. Aggleton, J.) 1–66 (Wiley-Liss, New York, 1992).

    Google Scholar 

  108. Freese, J. L. & Amaral, D. G. The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey. J.Comp. Neurol. 486, 295–317 (2005).

    PubMed  Google Scholar 

  109. Kveraga, K., Ghuman, A. S. & Bar, M. Top-down predictions in the cognitive brain. Brain Cogn. 65, 145–168 (2007).

    PubMed  PubMed Central  Google Scholar 

  110. MacDonald, A. W., 3rd, Cohen, J. D., Stenger, V. A. & Carter, C. S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 1835–1838 (2000).

    CAS  PubMed  Google Scholar 

  111. Kerns, J. G., et al. Anterior Cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026 (2004).

    CAS  PubMed  Google Scholar 

  112. Brown, J. W. & Braver, T. S. Learned predictions of error likelihood in the anterior cingulate cortex. Science 307, 1118–1121 (2005).

    CAS  PubMed  Google Scholar 

  113. Mesulam, M. M. A cortical network for directed attention and unilateral neglect. Ann. Neurol. 10, 309–325 (1981).

    CAS  PubMed  Google Scholar 

  114. Miltner, W. H. R., Braun, C. H. & Coles, G. H. Event-related brain potentials following incorrect feedback in a time-estimation task: Evidence for a 'generic' neural system for error-detection. J. Cogn. Neurosci. 9, 788–798 (1997).

    CAS  PubMed  Google Scholar 

  115. Schoenbaum, G., Roesch, M. R. & Stalnaker, T. A. Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci. 29, 116–124 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Zald, D. H. & Rauch, S. L. The orbitofrontal cortex (Oxford University Press, Oxford, 2007).

    Google Scholar 

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

    CAS  Google Scholar 

  118. Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259–288 (2007).

    CAS  PubMed  Google Scholar 

  119. Lewis, M. D. Bridging emotion theory and neurobiology through dynamic systems modeling. Behav. Brain Sci. 28, 169–194; discussion 194–245 (2005).

    PubMed  Google Scholar 

  120. Amiez, C., Joseph, J. P. & Procyk, E. Reward encoding in the monkey anterior cingulate cortex. Cereb. Cortex 16, 1040–1055 (2006).

    CAS  PubMed  Google Scholar 

  121. 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  PubMed  PubMed Central  Google Scholar 

  122. 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  PubMed  PubMed Central  Google Scholar 

  123. Rudebeck, P. H., Walton, M. E., Smyth, A. N., Bannerman, D. M. & Rushworth, M. F. Separate neural pathways process different decision costs. Nature Neurosci. 9, 1161–1168 (2006).

    CAS  PubMed  Google Scholar 

  124. Rushworth, M. F., Behrens, T. E., Rudebeck, P. H. & Walton, M. E. Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour. Trends Cogn. Sci. 11, 168–176 (2007).

    CAS  PubMed  Google Scholar 

  125. Zelazo, P. D. & Cunningham, W. A. Executive function: Mechanisms underlying emotion regulation in Handbook of emotion regulation (ed. Gross, J.) (Guilford, New York, 2007).

    Google Scholar 

  126. Mesulam, M. M. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann. Neurol. 28, 597–613 (1990).

    CAS  PubMed  Google Scholar 

  127. Mesulam, M. M. From sensation to cognition. Brain 121, 1013–1052 (1998).

    PubMed  Google Scholar 

  128. McIntosh, A. R. Towards a network theory of cognition. Neural Netw. 13, 861–870 (2000).

    CAS  PubMed  Google Scholar 

  129. Friston, K. Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Annu. Rev. Neurosci. 25, 221–250 (2002).

    CAS  PubMed  Google Scholar 

  130. Young, M. P., Hilgetag, C. C. & Scannell, J. W. On imputing function to structure from the behavioural effects of brain lesions. Phil. Trans. R. Soc. Lond. 355, 147–161 (2000).

    CAS  Google Scholar 

  131. Noppeney, U., Friston, K. J. & Price, C. J. Degenerate neuronal systems sustaining cognitive functions. J. Anat. 205, 433–442 (2004).

    PubMed  PubMed Central  Google Scholar 

  132. Price, C. J. & Friston, K. J. Degeneracy and cognitive anatomy. Trends Cogn. Sci. 6, 416–421 (2002).

    PubMed  Google Scholar 

  133. Damasio, A. The brain binds entities and events by multiregional activation from convergence zones. Neural Comput. 1, 123–132 (1989).

    Google Scholar 

  134. Passingham, R. E., Stephan, K. E. & Kotter, R. The anatomical basis of functional localization in the cortex. Nature Rev. Neurosci. 3, 606–616 (2002).

    CAS  Google Scholar 

  135. Guimera, R. & Nunes Amaral, L. A. Functional cartography of complex metabolic networks. Nature 433, 895–900 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Guimera, R., Sales-Pardo, M. & Amaral, L. A. N. Classes of complex networks defined by role-to-role connectivity profiles. Nature Phys. 3, 63–69 (2007).

    CAS  Google Scholar 

  137. Sporns, O., Honey, C. J. & Kotter, R. Identification and classification of hubs in brain networks. PLoS ONE 2, e1049. doi:1010.1371/journal.pone.00001049 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Bassett, D. S., Meyer-Lindenberg, A., Achard, S., Duke, T. & Bullmore, E. Adaptive reconfiguration of fractal small-world human brain functional networks. Proc. Natl Acad. Sci. USA 103, 19518–19523 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Achard, S., Salvador, R., Whitcher, B., Suckling, J. & Bullmore, E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26, 63–72 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Varela, F., Lachaux, J. P., Rodriguez, E. & Martinerie, J. The brainweb: phase synchronization and large-scale integration. Nature Rev. Neurosci. 2, 229–239 (2001).

    CAS  Google Scholar 

  141. Thompson, E. & Varela, F. J. Radical embodiment: neural dynamics and consciousness. Trends Cogn. Sci. 5, 418–425 (2001).

    PubMed  Google Scholar 

  142. Buzsáki, G. Rhythms of the brain (Oxford University Press, New York, 2006).

    Google Scholar 

  143. Honey, C. J., Kotter, R., Breakspear, M. & Sporns, O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl Acad. Sci. USA 104, 10240–10245 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Edelman, G. M. & Gally, J. A. Degeneracy and complexity in biological systems. Proc. Natl Acad. Sci. USA 98, 13763–13768 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Cahill, L., Weinberger, N. M., Roozendaal, B. & McGaugh, J. L. Is the amygdala a locus of “conditioned fear”? Some questions and caveats. Neuron 23, 227–228 (1999).

    CAS  PubMed  Google Scholar 

  146. Barrett, L. F. What is an emotion? (Guilford, New York, 2008).

    Google Scholar 

  147. Bechtel, W. & Richardson, R. C. Discovering complexity: Decomposition and localization as strategies in scientific research (Princeton University Press, Princeton, NJ, 1993).

  148. Simon, H. The sciences of the artificial (MIT Press, Cambridge, MA, 1969).

    Google Scholar 

  149. Thompson, E. Mind in life: Biology, Phenomenology, and the sciences of the mind (Harvard University Press, Cambridge, MA, 2007).

    Google Scholar 

  150. Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R. & Hirsch, J. Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51, 871–882 (2006).

    CAS  PubMed  Google Scholar 

  151. Goel, V. & Dolan, R. J. Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning. Neuroimage 20, 2314–2321 (2003).

    PubMed  Google Scholar 

  152. Dolcos, F. & McCarthy, G. Brain systems mediating cognitive interference by emotional distraction. J. Neurosci. 26, 2072–2079 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Northoff, G., et al. Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional-cognitive interaction. Hum. Brain Mapp. 21, 202–212 (2004).

    PubMed  PubMed Central  Google Scholar 

  154. Lashley, K. S. Basic neural mechanisms in behavior. Psych Rev. 37, 1–24 (1930).

    Google Scholar 

  155. Kotter, R. & Meyer, N. The limbic system: a review of its empirical foundation. Behav. Brain Res. 52, 105–127 (1992).

    CAS  PubMed  Google Scholar 

  156. Morgane, P. J. & Mokler, D. J. The limbic brain: continuing resolution. Neurosci. Biobehav Rev. 30, 119–125 (2006).

    PubMed  Google Scholar 

  157. Kaada, B. Cingulate, posterior orbital, anterior insular and temporal pole cortex in Handbook of physiology, Sect. 1. Neurophysiology (ed. Field, J., Magoun, H. W. & Hall, V. E.) 1345–1372 (Am. Physiol. Soc., Washington, DC, 1960).

    Google Scholar 

  158. Brodal, A. Neurological anatomy in relation to clinical medicine (Oxford University Press, New York, 1969).

    Google Scholar 

  159. Parkinson, B. & Colman, A. M. eds Emotion and motivation (Longman, London and New York, 1995).

    Google Scholar 

  160. Kuhl, J. Motivation and information processing: A new look at decision making, dynamic change, and action control in Handbook of motivation and cognition: Foundations of social behavior (ed. Sorrentino, R. M. & Higgins, E. T.) 404–434 (Wiley, Chichester, 1986).

    Google Scholar 

  161. Watanabe, M. Prefrontal unit activity during associative learning in monkey. Exp. Brain Res. 80, 296–309 (1990).

    CAS  PubMed  Google Scholar 

  162. Watanabe, M. Reward expectancy in primate prefrontal neurons. Nature 382, 629–632 (1996).

    CAS  PubMed  Google Scholar 

  163. Leon, M. I. & Shadlen, M. N. Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 24, 415–425 (1999).

    CAS  PubMed  Google Scholar 

  164. Tsujimoto, S. & Sawaguchi, T. Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex. J. Neurophysiol. 93, 3687–3692 (2005).

    PubMed  Google Scholar 

  165. Roesch, M. R. & Olson, C. R. Neuronal activity dependent on anticipated and elapsed delay in macaque prefrontal cortex, frontal and supplementary eye fields, and premotor cortex. J. Neurophysiol. 94, 1469–1497 (2005).

    PubMed  Google Scholar 

  166. Kobayashi, S., Lauwereyns, J., Koizumi, M., Sakagami, M. & Hikosaka, O. Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. J. Neurophysiol. 87, 1488–1498 (2002).

    PubMed  Google Scholar 

  167. Kobayashi, S. et al. Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward. Exp. Brain Res. 176, 341–355 (2007).

    PubMed  Google Scholar 

  168. Watanabe, M. Integration across multiple cognitive and motivational domains in monkey prefrontal cortex in Principles of frontal lobe function (eds Stuss, D. T. & Knight,R. T.) 326–337 (Oxford University Press, New York, 2002).

    Google Scholar 

  169. Watanabe, M. Role of anticipated reward in cognitive behavioral control. Curr.Op. Neurobiol. 17, 213–219 (2007).

    CAS  PubMed  Google Scholar 

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Acknowledgements

In the preparation of this article, I greatly benefited from feedback from and discussions with H. Barbas, L. Feldman Barrett, J. Moll, L. Oliveira, M. Pereira, A. Seth, O. Sporns, E. Thompson and R. Todd. I would also like to thank the reviewers for their constructive feedback and the National Institute of Mental Health (MH071589) for supporting my research.

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  1. Luiz Pessoa is at the Department of Psychological and Brain Sciences, and Programs in Neuroscience and Cognitive Science, Indiana University, Bloomington, Indiana 47405, USA. lpessoa@indiana.edu,

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Pessoa, L. On the relationship between emotion and cognition. Nat Rev Neurosci 9, 148–158 (2008). https://doi.org/10.1038/nrn2317

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