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Co-occurring anxiety influences patterns of brain activity in depression

  • Anna S. EngelsEmail author
  • Wendy Heller
  • Jeffrey M. Spielberg
  • Stacie L. Warren
  • Bradley P. Sutton
  • Marie T. Banich
  • Gregory A. Miller
Article

Abstract

Brain activation associated with anhedonic depression and co-occurring anxious arousal and anxious apprehension was measured by fMRI during performance of an emotion word Stroop task. Consistent with EEG findings, depression was associated with rightward frontal lateralization in the dorsolateral prefrontal cortex (DLPFC), but only when anxious arousal was elevated and anxious apprehension was low. Activity in the right inferior frontal gyrus (IFG) was also reduced for depression under the same conditions. In contrast, depression was associated with more activity in the anterior cingulate cortex (dorsal ACC and rostral ACC) and the bilateral amygdala. Results imply that depression, particularly when accompanied by anxious arousal, may result in a failure to implement top-down processing by appropriate brain regions (left DLPFC, right IFG) due to increased activation in regions associated with responding to emotionally salient information (right DLPFC, amygdala).

Keywords

Neutral Word Left DLPFC Anxious Arousal Penn State Worry Questionnaire Emotional Stroop Task 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aguirre, G. K., Zarahn, E., & D’Esposito, M. (1998). The variability of human, BOLD hemodynamic responses. NeuroImage, 8, 360–369. doi:10.1006/nimg.1998.0369CrossRefPubMedGoogle Scholar
  2. Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.Google Scholar
  3. Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116. doi:10.1038/nn1003CrossRefPubMedGoogle Scholar
  4. Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8, 170–177. doi:10.1016/j.tics.2004.02.010CrossRefPubMedGoogle Scholar
  5. Banich, M. T., Mackiewicz, K. L., Depue, B. E., Whitmer, A. J., Miller, G. A., & Heller, W. (2009). Cognitive control mechanisms, emotion and memory: A neural perspective with implications for psychopathology. Neuroscience & Biobehavioral Reviews, 33, 613–630. doi:10.1016/j.neubiorev.2008.09.010CrossRefGoogle Scholar
  6. Banich, M. T., Milham, M. P., Atchley, R. A., Cohen, N. J., Webb, A., Wszalek, T., et al. (2000). Prefrontal regions play a predominant role in imposing an attentional “set”: Evidence from fMRI. Cognitive Brain Research, 10, 1–9. doi:10.1016/S0926-6410(00)00015-XCrossRefPubMedGoogle Scholar
  7. Bear, D. M. (1986). Hemispheric asymmetries in emotional function: A reflection of lateral specialization in cortical-limbic connections. In B. K. Doane & K. E. Livingston (Eds.), The limbic system: Functional organization and clinical disorders (pp. 29–42). New York: Raven.Google Scholar
  8. Bench, C. J., Friston, K. J., Brown, R. G., Frackowiak, R. S. J., & Dolan, R. J. (1993). Regional cerebral blood flow in depression measured by positron emission tomography: The relationship with clinical dimensions. Psychological Medicine, 23, 579–590.CrossRefPubMedGoogle Scholar
  9. Bermpohl, F., Fregni, F., Boggio, P. S., Thut, G., Northoff, G., Otachi, P. T. M., et al. (2006). Effect of low-frequency transcranial magnetic stimulation on an affective go/no-go task in patients with major depression: Role of stimulation site and depression severity. Psychiatry Research, 141, 1–13. doi:10.1016/j.psychres.2005.07.018CrossRefPubMedGoogle Scholar
  10. Botvinick, M. M. (2008). Hierarchical models of behavior and prefrontal function. Trends in Cognitive Sciences, 12, 201–208. doi:10.1016/j.tics.2008.02.009CrossRefPubMedGoogle Scholar
  11. Bradley, M. M., & Lang, P. J. (1999). Affective norms for English words (ANEW). Gainesville: University of Florida, NIMH Center for the Study of Emotion and Attention.Google Scholar
  12. Brown, T. A., Antony, M. M., & Barlow, D. H. (1995). Diagnostic comorbidity in panic disorder: Effect on treatment outcome and course of comorbid diagnoses following treatment. Journal of Consulting & Clinical Psychology, 63, 408–418. doi:10.1037/0022-006X.63.3.408CrossRefGoogle Scholar
  13. Brown, T. A., Campbell, L. A., Lehman, C. L., Grisham, J. R., & Mancill, R. B. (2001). Current and lifetime comorbidity of the DSM-IV anxiety and mood disorders in a large clinical sample. Journal of Abnormal Psychology, 110, 585–599. doi:10.1037/0021-843X.110.4.585CrossRefPubMedGoogle Scholar
  14. Bruder, G. E., Fong, R., Tenke, C. E., Leite, P., Towey, J. P., Stewart, J. E., et al. (1997). Regional brain asymmetries in major depression with or without an anxiety disorder: A quantitative electroencephalographic study. Biological Psychiatry, 41, 939–948. doi:10.1016/S0006-3223(96)00260-0CrossRefPubMedGoogle Scholar
  15. Bruder, G. E., Stewart, J. W., Tenke, C. E., McGrath, P. J., Leite, P., Bhattacharya, N., & Quitkin, F. M. (2001). Electroencephalographic and perceptual asymmetry differences between responders and nonresponders to an SSRI antidepressant. Biological Psychiatry, 49, 416–425. doi:10.1016/S0006-3223(00)01016-7CrossRefPubMedGoogle Scholar
  16. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4, 215–222. doi:10.1016/S1364-6613(00)01483-2CrossRefPubMedGoogle Scholar
  17. Coan, J. A., & Allen, J. J. B. (2004). Frontal EEG asymmetry as a moderator and mediator of emotion. Biological Psychology, 67, 7–50. doi:10.1016/j.biopsycho.2004.03.002CrossRefPubMedGoogle Scholar
  18. Compton, R. J., Banich, M. T., Mohanty, A., Milham, M. P., Herrington, J., Miller, G. A., et al. (2003). Paying attention to emotion: An fMRI investigation of cognitive and emotional Stroop tasks. Cognitive, Affective, & Behavioral Neuroscience, 3, 81–96. doi:10.3758/CABN.3.2.81CrossRefGoogle Scholar
  19. Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58, 306–324. doi:10.1016/j.neuron.2008.04.017CrossRefPubMedGoogle Scholar
  20. Davidson, R. J. (2004). What does the prefrontal cortex “do” in affect: Perspectives on frontal EEG asymmetry research. Biological Psychology, 67, 219–233. doi:10.1016/j.biopsycho.2004.03.008CrossRefPubMedGoogle Scholar
  21. Dawson, J. F., & Richter, A. W. (2006). Probing three-way interactions in moderated multiple regression: Development and application of a slope difference test. Journal of Applied Psychology, 91, 917–926. doi:10.1037/0021-9010.91.4.917CrossRefPubMedGoogle Scholar
  22. Deldin, P. J., Keller, J., Gergen, J. A., & Miller, G. A. (2000). Right-posterior face-processing anomaly in depression. Journal of Abnormal Psychology, 109, 116–121. doi:10.1037/0021-843X.109.1.116CrossRefPubMedGoogle Scholar
  23. Elliott, R., Rubinsztein, J. S., Sahakian, B. J., & Dolan, R. J. (2002). The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry, 59, 597–604. doi:10.1001/archpsyc.59.7.597CrossRefPubMedGoogle Scholar
  24. Engels, A. S., Heller, W., Mohanty, A., Herrington, J. D., Banich, M. T., Webb, A. G., & Miller, G. A. (2007). Specificity of regional brain activity in anxiety types during emotion processing. Psychophysiology, 44, 352–363. doi:10.1111/j.1469-8986.2007.00518.xCrossRefPubMedGoogle Scholar
  25. Fitzgerald, P. B., Oxley, T. J., Laird, A. R., Kulkarni, J., Egan, G. F., & Daskalakis, Z. J. (2006). An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression. Psychiatry Research, 148, 33–45. doi:10.1016/j.psychresns.2006.04.006CrossRefPubMedGoogle Scholar
  26. Gaynes, B. N., Magruder, K. M., Burns, B. J., Wagner, H. R., Yarnall, K. S. H., & Broadhead, W. E. (1999). Does a coexisting anxiety disorder predict persistence of depressive illness in primary care patients with major depression? General Hospital Psychiatry, 21, 158–167. doi:10.1016/S0163-8343(99)00005-5CrossRefPubMedGoogle Scholar
  27. George, M. S., Ketter, T. A., Parekh, P. I., Rosinsky, N., Ring, H. A., Pazzaglia, P. J., et al. (1997). Blunted left cingulate activation in mood disorder subjects during a response interference task (the Stroop). Journal of Neuropsychiatry & Clinical Neurosciences, 9, 55–63.Google Scholar
  28. Ghaziuddin, N., King, C. A., Naylor, M. W., & Ghaziuddin, M. (2000). Anxiety contributes to suicidality in depressed adolescents. Depression & Anxiety, 11, 134–138. doi:10.1002/(SICI)1520-6394(2000)11:3<134::AID-DA9>3.0.CO;2-VCrossRefPubMedGoogle Scholar
  29. Heller, W. (1990). The neuropsychology of emotion: Developmental patterns and implications for psychopathology. In N. Stein, B. L. Leventhal, & T. Trabasso (Eds.), Psychological and biological approaches to emotion (pp. 167–211). Hillsdale, NJ: Erlbaum.Google Scholar
  30. Heller, W. (1993). Neuropsychological mechanisms of individual differences in emotion, personality, and arousal. Neuropsychology, 7, 476–489. doi:10.1037/0894-4105.7.4.476CrossRefGoogle Scholar
  31. Heller, W., & Nitschke, J. B. (1998). The puzzle of regional brain activity in depression and anxiety: The importance of subtypes and comorbidity. Cognition & Emotion, 12, 421–447. doi:10.1080/026999398379664CrossRefGoogle Scholar
  32. Heller, W., Nitschke, J. B., Etienne, M. A., & Miller, G. A. (1997). Patterns of regional brain activity differentiate types of anxiety. Journal of Abnormal Psychology, 106, 376–385. doi:10.1037/0021-843X.106.3.376CrossRefPubMedGoogle Scholar
  33. Herrington, J. D., Heller, W., Mohanty, A., Engels, A. S., Banich, M. T., Webb, A. G., & Miller, G. A. (in press). Localization of asymmetric brain function in emotion and depression. Psychophysiology. doi:10.1111/j.1469-8986.2009.00958.xGoogle Scholar
  34. Herrington, J. D., Mohanty, A., Koven, N. S., Fisher, J. E., Stewart, J. L., Banich, M. T., et al. (2005). Emotion-modulated performance and activity in left dorsolateral prefrontal cortex. Emotion, 5, 200–207. doi:10.1037/1528-3542.5.2.200CrossRefPubMedGoogle Scholar
  35. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841. doi:10.1016/S1053-8119(02)91132-8CrossRefPubMedGoogle Scholar
  36. Jenkinson, M., & Smith, S. (2001). A global optimization method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156. doi:10.1016/S1361-8415(01)00036-6CrossRefPubMedGoogle Scholar
  37. Jezzard, P., & Balaban, R. S. (1995). Correction for geometric distortion in echo planar images from B0 field variations. Magnetic Resonance in Medicine, 34, 65–73. doi:10.1002/mrm.1910340111CrossRefPubMedGoogle Scholar
  38. Johnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., & Davidson, R. J. (2007). Failure to regulate: Counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience, 27, 8877–8884. doi:10.1523/JNEUROSCI.2063-07.2007CrossRefPubMedGoogle Scholar
  39. Joormann, J., Kosfelder, J., & Schulte, D. (2005). The impact of comorbidity of depression on the course of anxiety treatments. Cognitive Therapy & Research, 29, 569–591. doi:10.1007/s10608-005-3340-5CrossRefGoogle Scholar
  40. Keller, J., Nitschke, J. B., Bhargava, T., Deldin, P. J., Gergen, J. A., Miller, G. A., & Heller, W. (2000). Neuropsychological differentiation of depression and anxiety. Journal of Abnormal Psychology, 109, 3–10. doi:10.1037/0021-843X.109.1.3CrossRefPubMedGoogle Scholar
  41. Kentgen, L. M., Tenke, C. E., Pine, D. S., Fong, R., Klein, R. G., & Bruder, G. E. (2000). Electroencephalographic asymmetries in adolescents with major depression: Influence of comorbidity with anxiety disorders. Journal of Abnormal Psychology, 109, 797–802. doi:10.1037/0021-843X.109.4.797CrossRefPubMedGoogle Scholar
  42. Kessler, R. C., Chiu, W. T., Demler, O., & Walters, E. E. (2005). Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 617–627. doi:10.1001/archpsyc.62.6.617CrossRefPubMedGoogle Scholar
  43. Kessler, R. C., Dupont, R. L., Berglund, P., & Wittchen, H.-U. (1999). Impairment in pure and comorbid generalized anxiety disorder and major depression at 12 months in two national surveys. American Journal of Psychiatry, 156, 1915–1923.PubMedGoogle Scholar
  44. Levin, R. L., Heller, W., Mohanty, A., Herrington, J. D., & Miller, G. A. (2007). Cognitive deficits in depression and functional specificity of regional brain activity. Cognitive Therapy & Research, 31, 211–233. doi:10.1007/s10608-007-9128-zCrossRefGoogle Scholar
  45. Maddock, R. J. (1999). The retrosplenial cortex and emotion: New insights from functional neuroimaging of the human brain. Trends in Neurosciences, 22, 310–316. doi:10.1016/S0166-2236(98)01374-5CrossRefPubMedGoogle Scholar
  46. Maddock, R. J., & Buonocore, M. H. (1997). Activation of left posterior cingulate gyrus by the auditory presentation of threat-related words: An fMRI study. Psychiatry Research, 75, 1–4. doi:10.1016/S0925-4927(97)00018-8CrossRefPubMedGoogle Scholar
  47. Maddock, R. J., Buonocore, M. H., Kile, S. J., & Garrett, A. S. (2003). Brain regions showing increased activation by threat-related words in panic disorder. NeuroReport, 14, 325–328. doi:10.1097/00001756-200303030-00006CrossRefPubMedGoogle Scholar
  48. Maddock, R. J., Garrett, A. S., & Buonocore, M. H. (2003). Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Human Brain Mapping, 18, 30–41. doi:10.1002/hbm.10075CrossRefPubMedGoogle Scholar
  49. McGuire, P. K., Bench, C. J., Frith, C. D., Marks, I. M., Frackowiak, R. S. J., & Dolan, R. J. (1994). Functional anatomy of obsessive-compulsive phenomena. British Journal of Psychiatry, 164, 459–468. doi:10.1192/bjp.164.4.459CrossRefPubMedGoogle Scholar
  50. Meyer, T. J., Miller, M. L., Metzger, R. L., & Borkovec, T. D. (1990). Development and validation of the Penn State Worry Questionnaire. Behaviour Research & Therapy, 28, 487–495. doi:10.1016/0005-7967(90)90135-6CrossRefGoogle Scholar
  51. Miezin, F. M., Maccotta, L., Ollinger, J. M., Petersen, S. E., & Buckner, R. L. (2000). Characterizing the hemodynamic response: Effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. NeuroImage, 11, 735–739. doi:10.1006/nimg.2000.0568CrossRefPubMedGoogle Scholar
  52. Milham, M. P., Erickson, K. I., Banich, M. T., Kramer, A. F., Webb, A., Wszalek, T., & Cohen, N. J. (2002). Attentional control in the aging brain: Insights from an fMRI study of the Stroop task. Brain & Cognition, 49, 277–296. doi:10.1006/brcg.2001.1501CrossRefGoogle Scholar
  53. Mineka, S., Watson, D., & Clark, L. A. (1998). Comorbidity of anxiety and unipolar mood disorders. Annual Review of Psychology, 49, 377–412. doi:10.1146/annurev.psych.49.1.377CrossRefPubMedGoogle Scholar
  54. Mitterschiffthaler, M. T., Williams, S. C. R., Walsh, N. D., Cleare, A. J., Donaldson, C., Scott, J., & Fu, C. H. Y. (2008). Neural basis of the emotional Stroop interference effect in major depression. Psychological Medicine, 38, 247–256. doi:10.1017/S0033291707001523CrossRefPubMedGoogle Scholar
  55. Mohanty, A., Engels, A. S., Herrington, J. D., Heller, W., Ho, M.-H. R., Banich, M. T., et al. (2007). Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function. Psychophysiology, 44, 343–351. doi:10.1111/j.1469-8986.2007.00515.xCrossRefPubMedGoogle Scholar
  56. Molina, S., & Borkovec, T. D. (1994). The Penn State Worry Questionnaire: Psychometric properties and associated characteristics. In G. C. L. Davey & F. Tallis (Eds.), Worrying: Perspectives on theory, assessment and treatment (pp. 265–283). Chichester, U.K.: Wiley.Google Scholar
  57. Nichols, T., Brett, M., Andersson, J., Wager, T., & Poline, J.-B. (2005). Valid conjunction inference with the minimum statistic. NeuroImage, 25, 653–660. doi:10.1016/j.neuroimage.2004.12.005CrossRefPubMedGoogle Scholar
  58. Nitschke, J. B., & Heller, W. (2005). Distinguishing neural substrates of heterogeneity among anxiety disorders. International Review of Neurobiology, 67, 1–42.CrossRefPubMedGoogle Scholar
  59. Nitschke, J. B., Heller, W., Imig, J. C., McDonald, R. P., & Miller, G. A. (2001). Distinguishing dimensions of anxiety and depression. Cognitive Therapy & Research, 25, 1–22. doi:10.1023/A:1026485530405CrossRefGoogle Scholar
  60. Nitschke, J. B., Heller, W., & Miller, G. A. (2000). Anxiety, stress, and cortical brain function. In J. C. Borod (Ed.), The neuropsychology of emotion (pp. 298–319). New York: Oxford.Google Scholar
  61. Nitschke, J. B., Heller, W., Palmieri, P. A., & Miller, G. A. (1999). Contrasting patterns of brain activity in anxious apprehension and anxious arousal. Psychophysiology, 36, 628–637. doi:10.1017/S0048577299972013CrossRefPubMedGoogle Scholar
  62. Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D. E., & Gross, J. J. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23, 483–499. doi:10.1016/j.neuroimage.2004.06.030CrossRefPubMedGoogle Scholar
  63. Pessoa, L., & Padmala, S. (2005). Quantitative prediction of perceptual decisions during near-threshold fear detection. Proceedings of the National Academy of Sciences, 102, 5612–5617. doi:10.1073/pnas.0500566102CrossRefGoogle Scholar
  64. Petrides, M. (2000). The role of the mid-dorsolateral prefrontal cortex in working memory. Experimental Brain Research, 133, 44–54. doi:10.1007/s002210000399CrossRefGoogle Scholar
  65. Petrides, M. (2005). Lateral prefrontal cortex: Architectonic and functional organization. Philosophical Transactions of the Royal Society B, 360, 781–795. doi:10.1098/rstb.2005.1631CrossRefGoogle Scholar
  66. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331–348. doi:10.1006/nimg.2002.1087CrossRefPubMedGoogle Scholar
  67. Pizzagalli, D. A., Nitschke, J. B., Oakes, T. R., Hendrick, A. M., Horras, K. A., Larson, C. L., et al. (2002). Brain electrical tomography in depression: The importance of symptom severity, anxiety, and melancholic features. Biological Psychiatry, 52, 73–85. doi:10.1016/S0006-3223(02)01313-6CrossRefPubMedGoogle Scholar
  68. Pizzagalli, D. A., Pascual-Marqui, R. D., Nitschke, J. B., Oakes, T. R., Larson, C. L., Abercrombie, H. C., et al. (2001). Anterior cingulate activity as a predictor of degree of treatment response in major depression: Evidence from brain electrical tomography analysis. American Journal of Psychiatry, 158, 405–415.CrossRefPubMedGoogle Scholar
  69. Reid, S. A., Duke, L. M., & Allen, J. J. B. (1998). Resting frontal electroencephalographic asymmetry in depression: Inconsistencies suggest the need to identify mediating factors. Psychophysiology, 35, 389–404. doi:10.1017/S0048577298970986CrossRefPubMedGoogle Scholar
  70. Sanderson, W. C., DiNardo, P. A., Rapee, R. M., & Barlow, D. H. (1990). Syndrome comorbidity in patients diagnosed with a DSM-III-R anxiety disorder. Journal of Abnormal Psychology, 99, 308–312.CrossRefPubMedGoogle Scholar
  71. Seghier, M. L. (2008). Laterality index in functional MRI: Methodological issues. Magnetic Resonance Imaging, 26, 594–601. doi:10.1016/j.mri.2007.10.010CrossRefPubMedGoogle Scholar
  72. Sherbourne, C. D., & Wells, K. B. (1997). Course of depression in patients with comorbid anxiety disorders. Journal of Affective Disorders, 43, 245–250. doi:10.1016/S0165-0327(97)01442-0CrossRefPubMedGoogle Scholar
  73. Silton, R. L., Heller, W., Towers, D. N., Engels, A. S., Edgar, J. C., Spielberg, J. M., et al. (2010). Depression and anxiety distinguish frontocingulate cortical activity during top-down attentional control. Manuscript under review.Google Scholar
  74. Toglia, M. P., & Battig, W. F. (1978). Handbook of semantic word norms. Hillsdale, NJ: Erlbaum.Google Scholar
  75. Ward, D. B. (2000). Simultaneous inference for FMRI data. Available at http://afni.nimh.nih.gov./pub/dist/doc/manual/AlphaSim.pdf; accessed July 27, 2006.Google Scholar
  76. Watson, D., Clark, L. A., Weber, K., Assenheimer, J. S., Strauss, M. E., & McCormick, R. A. (1995). Testing a tripartite model: II. Exploring the symptom structure of anxiety and depression in student, adult, and patient samples. Journal of Abnormal Psychology, 104, 15–25. doi:10.1037/0021-843X.104.1.15CrossRefPubMedGoogle Scholar
  77. Watson, D., Weber, K., Assenheimer, J. S., Clark, L. A., Strauss, M. E., & McCormick, R. A. (1995). Testing a tripartite model: I. Evaluating the convergent and discriminant validity of anxiety and depression symptom scales. Journal of Abnormal Psychology, 104, 3–14. doi:10.1037/0021-843X.104.1.3CrossRefPubMedGoogle Scholar
  78. Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of fMRI data. NeuroImage, 14, 1370–1386. doi:10.1006/nimg.2001.0931CrossRefPubMedGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2010

Authors and Affiliations

  • Anna S. Engels
    • 1
    • 2
    Email author
  • Wendy Heller
    • 2
  • Jeffrey M. Spielberg
    • 2
  • Stacie L. Warren
    • 2
  • Bradley P. Sutton
    • 2
  • Marie T. Banich
    • 3
  • Gregory A. Miller
    • 2
  1. 1.Social, Life, and Engineering Sciences Imaging CenterPennsylvania State UniversityUniversity Park
  2. 2.University of Illinois at Urbana-ChampaignUrbana
  3. 3.University of ColoradoBoulder

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