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Neuroanatomical Correlates of Executive Functions: A Neuropsychological Approach Using the EXAMINER Battery

Published online by Cambridge University Press:  13 June 2013

Heather Robinson ,
Matthew Calamia ,
Jan Gläscher ,
Joel Bruss  and
Daniel Tranel
Heather Robinson
Affiliation:
Department of Psychology, University of Iowa, Iowa City, Iowa
Matthew Calamia
Affiliation:
Department of Psychology, University of Iowa, Iowa City, Iowa
Jan Gläscher
Affiliation:
Department for Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Joel Bruss
Affiliation:
Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa
Daniel Tranel*
Affiliation:
Department of Psychology, University of Iowa, Iowa City, Iowa Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa
*
Correspondence and reprint requests to: Daniel Tranel, Department of Neurology, University of Iowa Hospitals and Clinics, 200 Hawkins Drive, Iowa City, Iowa 52242. E-mail: [email protected]
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Abstract

Executive functions (EF) encompass a variety of higher-order capacities such as judgment, planning, decision-making, response monitoring, insight, and self-regulation. Measuring such abilities quantitatively and establishing their neural correlates has proven to be challenging. Here, using a lesion-deficit approach, we report the neural correlates of a variety of EF tests that were developed under the auspices of the NINDS-supported EXAMINER project (Kramer, 2011; www.examiner.ucsf.edu). We administered a diverse set of EF tasks that tap three general domains—cognitive, social/emotional, and insight—to 37 patients with focal lesions to the frontal lobes, and 25 patients with lesions outside the frontal lobes. Using voxel-based lesion-symptom mapping (VLSM), we found that damage to the ventromedial prefrontal cortex (vmPFC) was predominately associated with deficits in social/emotional aspects of EF, while damage to dorsolateral prefrontal cortex (dlPFC) and anterior cingulate was predominately associated with deficits in cognitive aspects of EF. Evidence for an important role of some non-frontal regions (e.g., the temporal poles) in some aspects of EF was also found. The results provide further evidence for the neural basis of EF, and extend previous findings of the dissociation between the roles of the ventromedial and dorsolateral prefrontal sectors in organizing, implementing, and monitoring goal-directed behavior. (JINS, 2013, 19, 1–12)

Keywords

InsightSelf-monitoringFrSBeLesionCognitive controlEmpathy
Type
Special Series
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 1 , January 2014 , pp. 52 - 63
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

Adolphs, R., Damasio, H., Tranel, D., Damasio, A.R. (1996). Cortical systems for the recognition of emotion in facial expressions. The Journal of Neuroscience, 16(23), 7678–7687.CrossRefGoogle ScholarPubMed
Ames, D.L., Jenkins, A.C., Banaji, M.R., Mitchell, J.P. (2008). Taking another person's perspective increases self-referential neural processing. Psychological Science, 19, 642–644. doi:10.1111/j.1467-9280.2008.02135.x CrossRefGoogle ScholarPubMed
Ardila, A. (2008). On the evolutionary origins of executive functions. Brain and Cognition, 68, 92–99. doi:10.1016/j.bandc.2008.03.003 CrossRefGoogle ScholarPubMed
Arévalo, A.L., Baldo, J.V., Dronkers, N.F. (2012). What do brain lesions tell us about theories of embodied semantics and the human mirror neuron system? Cortex, 48, 242–254. doi:10.1016/j.cortex.2010.06.001 CrossRefGoogle ScholarPubMed
Barbey, A.K., Colom, R., Grafman, J. (2012). Dorsolateral prefrontal contributions to human intelligence. Neuropsychologia. [Epub ahead of print]. doi:10.1016/j.neuropsychologia.2012.05.017 Google ScholarPubMed
Barrash, J., Asp, E., Markon, K., Manzel, K., Anderson, S.W., Tranel, D. (2011). Dimensions of personality disturbance after focal brain damage: Investigation with the Iowa Scales of Personality Change. Journal of Clinical and Experimental Neuropsychology, 33, 833–852. doi:10.1080/13803395.2011.561300 CrossRefGoogle ScholarPubMed
Barrash, J., Tranel, D., Anderson, S.W. (2000). Acquired personality disturbances associated with bilateral damage to the ventromedial prefrontal region. Developmental Neuropsychology, 18, 355–381. doi:10.1207/S1532694205Barrash CrossRefGoogle Scholar
Bates, E., Wilson, S.M., Saygin, A.P., Dick, F., Sereno, M.I., Knight, R.T., Dronkers, N.F. (2003). Voxel-based lesion–symptom mapping. Nature Neuroscience, 6, 448–450. doi:10.1038/nn1050 CrossRefGoogle ScholarPubMed
Bechara, A. (2004). The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage. Brain and Cognition, 55, 30–40. doi:10.1016/j.bandc.2003.04.001 CrossRefGoogle ScholarPubMed
Bechara, A., Damasio, H., Damasio, A.R. (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex, 10, 295–307. doi:10.1093/cercor/10.3.295 CrossRefGoogle ScholarPubMed
Beer, J.S., John, O.P., Scabini, D., Knight, R.T. (2006). Orbitofrontal cortex and social behavior: Integrating self-monitoring and emotion-cognition interactions. Journal of Cognitive Neuroscience, 18, 871–879. doi:10.1162/jocn.2006.18.6.871 CrossRefGoogle ScholarPubMed
Berthoz, S., Armony, J.L., Blair, R.J.R., Dolan, R.J. (2002). An fMRI study of intentional and unintentional (embarrassing) violations of social norms. Brain, 125, 1696–1708. doi:10.1093/brain/awf190 CrossRefGoogle ScholarPubMed
Brunner, E., Munzel, U. (2000). The nonparametric Behrens-Fisher problem: Asymptotic theory and a small-sample approximation. Biometrical Journal, 42, 17–25. doi:10.1002/(SICI)1521-4036(200001)42:1<17::AID-BIMJ17>3.0.CO;2-U 3.0.CO;2-U>CrossRefGoogle Scholar
Chiaravalloti, N.D., DeLuca, J. (2003). Assessing the behavioral consequences of multiple sclerosis: An application of the Frontal Systems Behavior Scale (FrSBe). Cognitive and Behavioral Neurology, 16, 54–67. doi:10.1097/00146965-200303000-00007 CrossRefGoogle ScholarPubMed
Collette, F., Van der Linden, M., Laureys, S., Delfiore, G., Degueldre, C., Luxen, A., Salmon, E. (2005). Exploring the unity and diversity of the neural substrates of executive functioning. Human Brain Mapping, 25, 409–423. doi:10.1002/hbm.20118 CrossRefGoogle ScholarPubMed
Craig, A.D. (2011). Significance of the insula for the evolution of human awareness of feelings from the body. Annals of the New York Academy of Sciences, 1225, 72–82. doi:10.1111/j.1749-6632.2011.05990.x CrossRefGoogle ScholarPubMed
Damasio, A.R. (1994). Descartes’ error: Emotion, rationality and the human brain. New York: Putnam.Google Scholar
Damasio, A., Damasio, H., Tranel, D. (2013). Persistence of feelings and sentience after bilateral damage of the insula. Cerebral Cortex, 23, 833–846. doi:10.1093/cercor/bhs077 CrossRefGoogle ScholarPubMed
Davis, M.H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology; Journal of Personality and Social Psychology, 44(1), 113.CrossRefGoogle Scholar
Eslinger, P.J. (1998). Neurological and neuropsychological bases of empathy. European Neurology, 39, 193–199. doi:10.1159/000007933 CrossRefGoogle ScholarPubMed
Eslinger, P.J., Moore, P., Anderson, C., Grossman, M. (2011). Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. The Journal of Neuropsychiatry and Clinical Neurosciences, 23, 74–82. doi:10.1176/appi.neuropsych.23.1.74 CrossRefGoogle ScholarPubMed
Fiddick, L., Spampinato, M.V., Grafman, J. (2005). Social contracts and precautions activate different neurological systems: An fMRI investigation of deontic reasoning. Neuroimage, 28, 778–786. doi:10.1016/j.neuroimage.2005.05.033 CrossRefGoogle ScholarPubMed
Fiez, J.A., Damasio, H., Grabowski, T.J. (2000). Lesion segmentation and manual warping to a reference brain: Intra-and interobserver reliability. Human Brain Mapping, 9, 192–211. doi:10.1002/(SICI)1097-0193(200004)9:4<192::AID-HBM2>3.0.CO;2-Y 3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Frank, R.J., Damasio, H., Grabowski, T.J. (1997). Brainvox: An interactive, multimodal visualization and analysis system for neuroanatomical imaging. Neuroimage, 5, 13–30. doi:10.1006/nimg.1996.0250 CrossRefGoogle ScholarPubMed
Friston, K.J., Ashburner, J.T., Kiebel, S.J., Nichols, T.E., Penny, W.D. (Eds.). (2011). Statistical parametric mapping: The analysis of functional brain images: The analysis of functional brain images. New York: Academic Press.Google Scholar
Gläscher, J., Adolphs, R., Damasio, H., Bechara, A., Rudrauf, D., Calamia, M., Tranel, D. (2012). Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America, 109, 14681–14686. doi:10.1073/pnas.1206608109 CrossRefGoogle ScholarPubMed
Grace, J., Malloy, P. (2001). FrSBe, frontal systems behavior scale: Professional manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Grace, J., Stout, J.C., Malloy, P.F. (1999). Assessing frontal lobe behavioral syndromes with the frontal lobe personality scale. Assessment, 6, 269–284. doi:10.1177/107319119900600307 CrossRefGoogle ScholarPubMed
Hornberger, M., Geng, J., Hodges, J.R. (2011). Convergent grey and white matter evidence of orbitofrontal cortex changes related to disinhibition in behavioural variant frontotemporal dementia. Brain, 134, 2502–2512. doi:10.1093/brain/awr173 CrossRefGoogle ScholarPubMed
Kelley, W.M., Macrae, C.N., Wyland, C.L., Caglar, S., Inati, S., Heatherton, T.F. (2002). Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience, 14, 785–794. doi:10.1162/08989290260138672 CrossRefGoogle ScholarPubMed
Koenigs, M., Barbey, A.K., Postle, B.R., Grafman, J. (2009). Superior parietal cortex is critical for the manipulation of information in working memory. The Journal of Neuroscience, 29, 14980–14986. doi:10.1523/JNEUROSCI.3706-09.2009 CrossRefGoogle ScholarPubMed
Kramer, J. (2011). Executive abilities: Measures and instruments for neurobehavioral evaluation and research (EXAMINER). Retrieved from: http://examiner.ucsf.edu/EXAMINER%20User%20Manual.pdf Google Scholar
Latzman, R.D., Markon, K.E. (2010). The factor structure and age-related factorial invariance of the Delis-Kaplan Executive Function System (D-KEFS). Assessment, 17, 172–184. doi:10.1177/1073191109356254 CrossRefGoogle ScholarPubMed
Lennox, R.D., Wolfe, R.N. (1984). Revision of the self-monitoring scale. Journal of Personality and Social Psychology, 46, 1349–1364. doi:10.1037/0022-3514.46.6.1349 CrossRefGoogle ScholarPubMed
Levine, B., Stuss, D.T., Milberg, W.P., Alexander, M.P., Schwartz, M., Macdonald, R. (1998). The effects of focal and diffuse brain damage on strategy application: Evidence from focal lesions, traumatic brain injury and normal aging. Journal of the International Neuropsychological Society, 4, 247–264.CrossRefGoogle ScholarPubMed
Levy, R., Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex–basal ganglia circuits. Cerebral Cortex, 16, 916–928. doi:10.1093/cercor/bhj043 CrossRefGoogle ScholarPubMed
Lezak, M.D., Howieson, D.B., Bigler, E.D., Tranel, D. (2012). Neuropsychological assessment (5th ed.). New York: Oxford University Press.Google Scholar
Li, X., Lu, Z., D'Argembeau, A., Ng, M., Bechara, A. (2010). The Iowa Gambling Task in fMRI images. Human Brain Mapping, 31(3), 410–423. doi:10.1002/hbm.20875 CrossRefGoogle ScholarPubMed
Massimo, L., Libon, D.J., Chandrasekaran, K., Dreyfuss, M., McMillan, C.T., Rascovsky, K., Grossman, M. (2013). Self-appraisal in behavioural variant frontotemporal degeneration. Journal of Neurology, Neurosurgery, & Psychiatry, 84, 148–153. doi:10.1136/jnnp-2012-303153 CrossRefGoogle ScholarPubMed
Massimo, L., Powers, C., Moore, P., Vesely, L., Avants, B., Gee, J., Grossman, M. (2009). Neuroanatomy of apathy and disinhibition in frontotemporal lobar degeneration. Dementia and Geriatric Cognitive Disorders, 27, 96–104. doi:10.1159/000194658 CrossRefGoogle ScholarPubMed
Minzenberg, M.J., Laird, A.R., Thelen, S., Carter, C.S., Glahn, D.C. (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry, 66, 811. doi:10.1001/archgenpsychiatry.2009.91 CrossRefGoogle ScholarPubMed
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., Wager, T.D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychology, 41, 49–100. doi:10.1006/cogp.1999.0734 CrossRefGoogle ScholarPubMed
Northoff, G., Grimm, S., Boeker, H., Schmidt, C., Bermpohl, F., Heinzel, A., Boesiger, P. (2006). Affective judgment and beneficial decision making: Ventromedial prefrontal activity correlates with performance in the Iowa Gambling Task. Human Brain Mapping, 27(7), 572–587. doi:10.1002/hbm.20202 CrossRefGoogle ScholarPubMed
O'Doherty, J.P. (2004). Reward representations and reward-related learning in the human brain: Insights from neuroimaging. Current Opinion in Neurobiology, 14(6), 769–776. doi:10.1016/j.conb.2004.10.016 CrossRefGoogle ScholarPubMed
Philippi, C.L., Duff, M.C., Denburg, N.L., Tranel, D., Rudrauf, D. (2012). Medial PFC damage abolishes the self-reference effect. Journal of Cognitive Neuroscience, 24, 475–481. doi:10.1162/jocn_a_00138 CrossRefGoogle ScholarPubMed
Philippi, C.L., Feinstein, J.S., Khalsa, S.S., Damasio, A., Tranel, D., Landini, G., Rudrauf, D. (2012). Preserved self-awareness following extensive bilateral brain damage to the insula, anterior cingulate, and medial prefrontal cortices. PloS one, 7, e38413. doi:10.1371/journal.pone.0038413 CrossRefGoogle Scholar
Rorden, C., Karnath, H.O., Bonilha, L. (2007). Improving lesion-symptom mapping. Journal of Cognitive Neuroscience, 19, 1081–1088. doi:10.1162/jocn.2007.19.7.1081 CrossRefGoogle ScholarPubMed
Rosen, H.J., Alcantar, O., Rothlind, J., Sturm, V., Kramer, J.H., Weiner, M., Miller, B.L. (2010). Neuroanatomical correlates of cognitive self-appraisal in neurodegenerative disease. Neuroimage, 49, 3358–3364. doi:10.1016/j.neuroimage.2009.11.041 CrossRefGoogle ScholarPubMed
Saver, J.L., Damasio, A.R. (1991). Preserved access and processing of social knowledge in a patient with acquired sociopathy due to ventromedial frontal damage. Neuropsychologia, 29, 1241–1249. doi:10.1016/0028-3932(91)90037-9 CrossRefGoogle Scholar
Saygin, A.P. (2007). Superior temporal and premotor brain areas necessary for biological motion perception. Brain, 130, 2452–2461. doi:10.1093/brain/awm162 CrossRefGoogle ScholarPubMed
Shallice, T., Burgess, P.W. (1991). Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727–741. doi:10.1093/brain/114.2.727 CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S.G., Aharon-Peretz, J., Perry, D. (2009). Two systems for empathy: A double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain, 132, 617–627. doi:10.1093/brain/awn279 CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S.G., Tomer, R., Berger, B., Aharon-Peretz, J. (2003). Characterization of empathy deficits following prefrontal brain damage: The role of the right ventromedial prefrontal cortex. Journal of Cognitive Neuroscience, 15, 324–337. doi:10.1162/089892903321593063 CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S.G., Tomer, R., Goldsher, D., Berger, B.D., Aharon-Peretz, J. (2004). Impairment in cognitive and affective empathy in patients with brain lesions: Anatomical and cognitive correlates. Journal of Clinical and Experimental Neuropsychology, 26, 1113–1127. doi:10.1080/13803390490515531 CrossRefGoogle ScholarPubMed
Stuss, D.T. (2011). Functions of the frontal lobes: Relation to executive functions. Journal of the International Neuropsychological Society, 17, 759–765. doi:10.1017/S1355617711000695 CrossRefGoogle ScholarPubMed
Stuss, D.T., Alexander, M.P., Hamer, L., Palumbo, C., Dempster, R., Binns, M., Izukawa, D. (1998). The effects of focal anterior and posterior brain lesions on verbal fluency. Journal of the International Neuropsychological Society, 4(3), 265–278.CrossRefGoogle ScholarPubMed
Stuss, D.T., Knight, R.T. (Eds.). (2002). Principles of frontal lobe function. New York: Oxford University Press.CrossRefGoogle Scholar
Stuss, D., Levine, B. (2002). Adult clinical neuropsychology: Lessons from studies of the frontal lobes. Annual Review of Psychology, 53, 401–433. doi:10.1146/annurev.psych.53.100901.135220 CrossRefGoogle ScholarPubMed
Tranel, D., Anderson, S.W., Benton, A.L. (1994). Development of the concept of “executive function” and its relationship to the frontal lobes. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (Vol. 9, pp. 125–148). Amsterdam: Elsevier.Google Scholar
Tsujimoto, M., Senda, J., Ishihara, T., Niimi, Y., Kawai, Y., Atsuta, N., Sobue, G. (2011). Behavioral changes in early ALS correlate with voxel-based morphometry and diffusion tensor imaging. Journal of the Neurological Sciences, 307, 34–40. doi:10.1016/j.jns.2011.05.025 CrossRefGoogle ScholarPubMed
Van Breukelen, G.J.P., Vlaeyen, J.W.S. (2005). Norming clinical questionnaires with multiple regression: The pain cognition list. Psychological Assessment, 17, 336. doi:10.1037/1040-3590.17.3.336 CrossRefGoogle ScholarPubMed
Wallis, J.D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annual Review of Neuroscience, 30(1), 31–56. doi:10.1146/annurev.neuro.30.051606.094334 CrossRefGoogle ScholarPubMed
Zamboni, G., Huey, E., Krueger, F., Nichelli, P., Grafman, J. (2008). Apathy and disinhibition in frontotemporal dementia Insights into their neural correlates. Neurology, 71, 736–742. doi:10.1212/01.wnl.0000324920.96835.95 CrossRefGoogle ScholarPubMed