The Insular Cortex: Relationship to Skin Conductance Responses to Facial Expression of Emotion in Temporal Lobe Epilepsy

  • Sarah J. BanksEmail author
  • Jenny Bellerose
  • Danielle Douglas
  • Marilyn Jones-Gotman


The insula plays an important role both in emotion processing and in the generation of epileptic seizures. In the current study we examined thickness of insular cortices and bilateral skin conductance responses (SCR) in healthy subjects in addition to a small number of patients with temporal lobe epilepsy. SCR measures arousal and is used to assess non-conscious responses to emotional stimuli. We used two emotion tasks, one explicitly about emotion and the other implicit. The explicit task required judgments about emotions being expressed in photographs of faces, while the implicit one required judgments about the age of the people in the photographs. Patients and healthy differed in labeling neutral faces, but not other emotions. They also differed in their SCR to emotions, though the profile depended on which hand the recordings were from. Finally, we found relationships between the thickness of the insula and SCR to each task: in the healthy group the thickness of the left insula was related to SCR to the emotion-labeling task; in the patient group it was between the thickness of the right insula and SCR in the age-labeling task. These patterns were evident only for the right hand recordings, thus underscoring the importance of bilateral recordings.


Skin conductance response Insula Emotion Epilepsy 


  1. Adolphs, R., Tranel, D., & Damasio, H. (2001). Emotion recognition from faces and prosody following temporal lobectomy. Neuropsychology, 15(3), 396–404.PubMedCrossRefGoogle Scholar
  2. Banks, S. J., Bellerose, J., Douglas, D., & Jones-Gotman, M. (2012a). Bilateral skin conductance responses to emotional faces. Applied Psychophysiology and Biofeedback,. doi: 10.1007/s10484-011-9177-7.PubMedGoogle Scholar
  3. Banks, S. J., Sziklas, V., Sodums, D. J., & Jones-Gotman, M. (2012). fMRI of verbal and nonverbal memory processes in healthy and epileptogenic medial temporal lobes. [Research Support, Non-U.S. Gov’t]. Epilepsy and Behavior, 25(1), 42–49. doi: 10.1016/j.yebeh.2012.07.003.
  4. Bernhardt, B. C., Bernasconi, N., Concha, L., & Bernasconi, A. (2010). Cortical thickness analysis in temporal lobe epilepsy: Reproducibility and relation to outcome. Neurology, 74(22), 1776–1784. doi: 10.1212/WNL.0b013e3181e0f80a.PubMedCrossRefGoogle Scholar
  5. Borod, J. C. (1992). Interhemispheric and intrahemispheric control of emotion: A focus on unilateral brain damage. Journal of Consulting and Clinical Psychology, 60(3), 339–348.PubMedCrossRefGoogle Scholar
  6. Boucsein, W., Fowles, D. C., Grimnes, S., Ben-Shakhar, G., Roth, W. T., Dawson, M. E., et al. (2012). Publication recommendations for electrodermal measurements. [Guideline]. Psychophysiology, 49(8), 1017–1034. doi: 10.1111/j.1469-8986.2012.01384.x.PubMedGoogle Scholar
  7. Bouilleret, V., Dupont, S., Spelle, L., Baulac, M., Samson, Y., & Semah, F. (2002). Insular cortex involvement in mesiotemporal lobe epilepsy: A positron emission tomography study. Annals of Neurology, 51(2), 202–208. doi: 10.1002/ana.10087.PubMedCrossRefGoogle Scholar
  8. Chen, Y. H., Dammers, J., Boers, F., Leiberg, S., Edgar, J. C., Roberts, T. P., et al. (2009). The temporal dynamics of insula activity to disgust and happy facial expressions: A magnetoencephalography study. Neuroimage, 47(4), 1921–1928. doi: 10.1016/j.neuroimage.2009.04.093.PubMedCrossRefGoogle Scholar
  9. Cooney, R. E., Atlas, L. Y., Joormann, J., Eugene, F., & Gotlib, I. H. (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: Is neutral really neutral? Psychiatry Research, 148(1), 55–59. doi: 10.1016/j.pscychresns.2006.05.003.PubMedCrossRefGoogle Scholar
  10. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. [Research Support, Non-U.S. Gov’t]. Nature Reviews Neuroscience, 10(1), 59–70. doi: 10.1038/nrn2555.
  11. Crespo-Facorro, B., Kim, J., Andreasen, N. C., O’Leary, D. S., Bockholt, H. J., & Magnotta, V. (2000). Insular cortex abnormalities in schizophrenia: A structural magnetic resonance imaging study of first-episode patients. Schizophrenia Research, 46(1), 35–43.PubMedCrossRefGoogle Scholar
  12. Critchley, H. D., Elliott, R., Mathias, C. J., & Dolan, R. J. (2000). Neural activity relating to generation and representation of galvanic skin conductance responses: A functional magnetic resonance imaging study. The Journal of Neuroscience: the Official Journal of the SOCIETY for Neuroscience, 20(8), 3033–3040.Google Scholar
  13. Damasio, A. R. (1996). The somatic marker hypothesis and the possible functions of the prefrontal cortex. [Research Support, U.S. Gov’t, P.H.S. Review]. Philosophical Transactions of the Royal Society of London: B Biological Sciences, 351(1346), 1413–1420. doi: 10.1098/rstb.1996.0125.
  14. Damasio, A., Damasio, H., & Tranel, D. (2013). Persistence of feelings and sentience after bilateral damage of the insula. [Case Reports Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Cerebral Cortex, 23(4), 833–846. doi: 10.1093/cercor/bhs077.
  15. Davidson, R. J., & Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Science, 3(1), 11–21.CrossRefGoogle Scholar
  16. Edwards, J., Jackson, H. J., & Pattison, P. E. (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review, 22(6), 789–832.PubMedCrossRefGoogle Scholar
  17. Fowler, H. L., Baker, G. A., Tipples, J., Hare, D. J., Keller, S., Chadwick, D. W., et al. (2006). Recognition of emotion with temporal lobe epilepsy and asymmetrical amygdala damage. Epilepsy & Behavior, 9(1), 164–172. doi: 10.1016/j.yebeh.2006.04.013.CrossRefGoogle Scholar
  18. Glascher, J., & Adolphs, R. (2003). Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. Journal of Neuroscience, 23(32), 10274–10282.PubMedGoogle Scholar
  19. Gur, R. C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., et al. (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods, 115(2), 137–143.PubMedCrossRefGoogle Scholar
  20. Habel, U., Windischberger, C., Derntl, B., Robinson, S., Kryspin-Exner, I., Gur, R. C., & Moser, E. (2007). Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Neuropsychologia, 45(10), 2369–2377. doi: 10.1016/j.neuropsychologia.2007.01.023.
  21. Isnard, J., Guenot, M., Ostrowsky, K., Sindou, M., & Mauguiere, F. (2000). The role of the insular cortex in temporal lobe epilepsy. Annals of Neurology, 48(4), 614–623.PubMedCrossRefGoogle Scholar
  22. Jack, C. R, Jr, Bernstein, M. A., Fox, N. C., Thompson, P., Alexander, G., Harvey, D., et al. (2008). The Alzheimer’s Disease Neuroimaging Initiative (ADNI): MRI methods. [Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, P.H.S.]. Journal of Magnetic Resononance Imaging, 27(4), 685–691. doi: 10.1002/jmri.21049.CrossRefGoogle Scholar
  23. Jalava, M., Sillanpaa, M., Camfield, C., & Camfield, P. (1997). Social adjustment and competence 35 years after onset of childhood epilepsy: A prospective controlled study. Epilepsia, 38(6), 708–715.PubMedCrossRefGoogle Scholar
  24. Jehna, M., Neuper, C., Ischebeck, A., Loitfelder, M., Ropele, S., Langkammer, C., et al. (2011). The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI. Brain Research, 1393, 73–83. doi: 10.1016/j.brainres.2011.04.007.PubMedCrossRefGoogle Scholar
  25. Lamm, C., & Singer, T. (2010). The role of anterior insular cortex in social emotions. Brain Structure and Function, 214(5–6), 579–591. doi: 10.1007/s00429-010-0251-3.PubMedCrossRefGoogle Scholar
  26. Lane, R. D., Reiman, E. M., Bradley, M. M., Lang, P. J., Ahern, G. L., Davidson, R. J., et al. (1997). Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia, 35(11), 1437–1444.PubMedCrossRefGoogle Scholar
  27. Leppanen, J. M., Milders, M., Bell, J. S., Terriere, E., & Hietanen, J. K. (2004). Depression biases the recognition of emotionally neutral faces. Psychiatry Research, 128(2), 123–133. doi: 10.1016/j.psychres.2004.05.020.PubMedCrossRefGoogle Scholar
  28. Liberzon, I., Taylor, S. F., Fig, L. M., Decker, L. R., Koeppe, R. A., & Minoshima, S. (2000). Limbic activation and psychophysiologic responses to aversive visual stimuli. Interaction with cognitive task. Neuropsychopharmacology, 23(5), 508–516. doi: 10.1016/S0893-133X(00)00157-3.PubMedCrossRefGoogle Scholar
  29. Lough, S., Kipps, C. M., Treise, C., Watson, P., Blair, J. R., & Hodges, J. R. (2006). Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia, 44(6), 950–958. doi: 10.1016/j.neuropsychologia.2005.08.009.PubMedCrossRefGoogle Scholar
  30. Mangina, C. A., & Beuzeron-Mangina, J. H. (1996). Direct electrical stimulation of specific human brain structures and bilateral electrodermal activity. International Journal of Psychophysiology, 22(1–2), 1–8.PubMedCrossRefGoogle Scholar
  31. Meletti, S., Benuzzi, F., Cantalupo, G., Rubboli, G., Tassinari, C. A., & Nichelli, P. (2009). Facial emotion recognition impairment in chronic temporal lobe epilepsy. Epilepsia, 50(6), 1547–1559. doi: 10.1111/j.1528-1167.2008.01978.x.PubMedCrossRefGoogle Scholar
  32. Meletti, S., Benuzzi, F., Rubboli, G., Cantalupo, G., Stanzani Maserati, M., Nichelli, P., et al. (2003). Impaired facial emotion recognition in early-onset right mesial temporal lobe epilepsy. Neurology, 60(3), 426–431.PubMedCrossRefGoogle Scholar
  33. Mesulam, M. M., & Mufson, E. J. (1982). Insula of the old world monkey. III: Efferent cortical output and comments on function. Journal of Comparative Neurology, 212(1), 38–52. doi: 10.1002/cne.902120104.PubMedCrossRefGoogle Scholar
  34. Nguyen, D. K., Nguyen, D. B., Malak, R., Leroux, J. M., Carmant, L., Saint-Hilaire, J. M., et al. (2009). Revisiting the role of the insula in refractory partial epilepsy. Epilepsia, 50(3), 510–520. doi: 10.1111/j.1528-1167.2008.01758.x.PubMedCrossRefGoogle Scholar
  35. 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(2), 331–348. doi: 10.1006/nimg.2002.1087.PubMedCrossRefGoogle Scholar
  36. Rosen, H. J., Gorno-Tempini, M. L., Goldman, W. P., Perry, R. J., Schuff, N., Weiner, M., et al. (2002). Patterns of brain atrophy in frontotemporal dementia and semantic dementia. Neurology, 58(2), 198–208.PubMedCrossRefGoogle Scholar
  37. Soussignan, R., Ehrle, N., Henry, A., Schaal, B., & Bakchine, S. (2005). Dissociation of emotional processes in response to visual and olfactory stimuli following frontotemporal damage. Neurocase, 11(2), 114–128. doi: 10.1080/13554790590922513.PubMedCrossRefGoogle Scholar
  38. Williams, L. M., Brown, K. J., Das, P., Boucsein, W., Sokolov, E. N., Brammer, M. J., et al. (2004). The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception. [Clinical Trial Research Support, Non-U.S. Gov’t]. Brain Research: Cognitive Brain Research, 21(1), 114–123. doi: 10.1016/j.cogbrainres.2004.06.005.PubMedGoogle Scholar
  39. Wright, P., He, G., Shapira, N. A., Goodman, W. K., & Liu, Y. (2004). Disgust and the insula: fMRI responses to pictures of mutilation and contamination. NeuroReport, 15(15), 2347–2351.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sarah J. Banks
    • 1
    Email author
  • Jenny Bellerose
    • 2
  • Danielle Douglas
    • 3
  • Marilyn Jones-Gotman
    • 4
  1. 1.Cleveland Clinic Lou Ruvo Center for Brain HealthLas VegasUSA
  2. 2.Université de MontrealMontrealCanada
  3. 3.University of TorontoTorontoCanada
  4. 4.McGill UniversityMontrealCanada

Personalised recommendations