Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-17T16:16:23.999Z Has data issue: false hasContentIssue false
  • English
  • Français

Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex

Published online by Cambridge University Press:  22 March 2006

STEVEN W. ANDERSON ,
JOSEPH BARRASH ,
ANTOINE BECHARA  and
DANIEL TRANEL
STEVEN W. ANDERSON
Affiliation:
Department of Neurology, University of Iowa Carver College of Medicine, Iowa City, Iowa
JOSEPH BARRASH
Affiliation:
Department of Neurology, University of Iowa Carver College of Medicine, Iowa City, Iowa VA Medical Center, Iowa City, Iowa
ANTOINE BECHARA
Affiliation:
Department of Neurology, University of Iowa Carver College of Medicine, Iowa City, Iowa
DANIEL TRANEL
Affiliation:
Department of Neurology, University of Iowa Carver College of Medicine, Iowa City, Iowa
Get access Rights & Permissions [Opens in a new window]

Abstract

The behavioral syndrome resulting from damage to the ventromedial prefrontal (VM) region presents major challenges for clinical assessment and management, stemming from the absence of reliable neurologic or psychometric markers, coupled with often debilitating impairments of decision-making and behavior regulation. Damage to this region disrupts neural circuitry critical for emotion, which in turn may contribute to impairments in real-world competencies. Here we present findings from patients with focal lesions in the VM region acquired either in childhood or adulthood, and show that there is a relationship between emotional dysfunction and impairments in real-world behavioral competencies. Emotion was rated by participants' relatives on dimensions including frustration tolerance, lability, anxiety, and blunted affect. Real-world competencies were rated by the relatives on dimensions including judgment, planning, and initiation, and were evaluated by clinician ratings in areas including social, financial, and occupational function. VM damage resulted in severe disruption of emotion, and this emotional dysfunction accounted for a significant portion of impaired real-world competencies. The long-term impairments associated with childhood-onset lesions were at least as severe as those resulting from adult-onset damage. Greater focus on the contribution of emotional dysfunction to the real-world competencies of patients with damage in the VM region may sharpen their neuropsychological assessment and facilitate rehabilitation efforts. (JINS, 2006, 12, 224–235.)

Keywords

Prefrontal cortexEmotionDecision-making
Type
SYMPOSIUM
Information
Journal of the International Neuropsychological Society , Volume 12 , Issue 2 , March 2006 , pp. 224 - 235
Copyright
© 2006 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ackerly, S.S. & Benton, A.L. (1947). Report of a case of bilateral frontal lobe defect. Research Publication of the Association for Research in Nervous and Mental Disease, 27, 479–504.Google Scholar
Anderson, S.W., Bechara, A., Damasio, H., Tranel, D., & Damasio, A.R. (1999). Impairment of social and moral behavior related to early damage in the human prefrontal cortex. Nature Neuroscience, 2, 1032–1037.Google Scholar
Anderson, S.W., Damasio, H., & Damasio, A.R. (2005). A neural basis for collecting behavior in humans. Brain, 128, 201–212.Google Scholar
Anderson, S.W., Damasio, H., Jones, R.D., & Tranel, D. (1991). Wisconsin Card Sorting Test performance as a measure of frontal lobe damage. Journal of Clinical and Experimental Neuropsychology, 13, 909–922.Google Scholar
Bar-On, R., Tranel, D., Denburg, N.L., & Bechara, A. (2003). Exploring the neurological substrates of emotional and social intelligence. Brain, 126, 1790–1800.Google Scholar
Barrash, J., Anderson, S.W., Jones, R.D., & Tranel, D. (1997). The Iowa Rating Scales of Personality Change: Reliability and validity. Journal of the International Neuropsychological Society, 3, 27–28 (abstract).Google Scholar
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.CrossRefGoogle Scholar
Bechara, A., Tranel, D., Damasio, H., & Damasio, A.R. (1996). Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cerebral Cortex, 6, 215–225.Google Scholar
Camille, N., Coricelli, G., Sallet, J., Pradat-Diehl, P., Duhamel, J.-R., & Sirigu, A. (2004). The involvement of the orbitofrontal cortex in the experience of regret. Science, 304, 1167–1170.Google Scholar
Damasio, A.R. (1994). Descartes' error: Emotion, reason, and the human brain. New York: Grosset/Putnam.
Damasio, A.R. & Anderson, S.W. (2003). The frontal lobes. In K.M. Heilman & E. Valenstein (Eds.), Clinical neuropsychology (4th ed.). New York: Oxford University Press.
Damasio, H. & Damasio, A.R. (1989). Lesion analysis in neuropsychology. New York: Oxford University Press.
Damasio, H. & Frank, R. (1992). Three-dimensional in vivo mapping of brain lesions in humans. Archives of Neurology, 49, 137–143.Google Scholar
Eslinger, P.J. (1998). Neurological and neuropsychological bases of empathy. European Neurology, 39, 193–199.Google Scholar
Eslinger, P.J. & Damasio, A.R. (1985). Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR. Neurology, 35, 1731–1741.Google Scholar
Eslinger, P.J., Flaherty-Craig, C.V., & Benton, A.L. (2004). Developmental outcomes after early prefrontal cortex damage. Brain and Cognition, 55, 84–103.Google Scholar
Eslinger, P.J., Grattan, L.M., & Damasio, A.R. (1992). Developmental consequences of childhood frontal lobe damage. Archives of Neurology, 49, 764–769.Google Scholar
Frank, R.J., Damasio, H., & Grabowski, T.J. (1997). Brainvox: An interactive, multimodal visualization and analyss system for neuroanatomical imaging. Neuroimage, 5, 13–30.Google Scholar
Frith, U. & Frith, C.D. (2003). Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society of London, 358, 459–473.Google Scholar
Grafman, J., Jonas, B., & Salazar, A. (1990). Wisconsin Card Sorting Test performance based on location and size of neuroanatomical lesion in Vietnam veterans with penetrating head injury. Perceptual and Motor Skills, 71, 1120–1122.Google Scholar
Gusnard, D.A., Akbudak, E., Shulman, G.L., & Raichle, M.E. (2001). Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proceedings of the National Academy of Science, 98, 4259–4264.Google Scholar
Happaney, K., Zelazo, P.D., & Stuss, D.T. (2004). Development of orbitofrontal function: Current themes and future directions. Brain and Cognition, 55, 1–10.Google Scholar
Harlow, J.M. (1868). Recovery from the passage of an iron bar through the head. Publication of the Massachusetts Medical Society, 2, 329–347.Google Scholar
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.Google Scholar
Machado, C.J. & Bachevalier, J. (2003). Non-human primate models of childhood psychopathology: The promise and the limitations. Journal of Child Psychology and Psychiatry, 44, 64–87.Google Scholar
Rolls, E.T., Hornak, J., Wade, D., & McGrath, J. (1994). Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery & Psychiatry, 57, 1518–1524.Google Scholar
Saver, J. & 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.Google Scholar
Siegert, R.J., McPherson, K.M., & Taylor, W.J. (2004). Toward a cognitive-affective model of goal-setting in rehabilitation: Is self-regulation theory a key step? Disability and Rehabilitation, 26, 1175–1183.Google Scholar
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.Google Scholar
Shallice, T. & Burgess, W.P. (1991). Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727–741.Google Scholar
Stuss, D.T. & Benson, D.F. (1986). The frontal lobes. New York: Raven Press.
Stuss, D.T. & Levine, B. (2002). Adult clinical neuropsychology: Lessons from studies of the frontal lobes. Annual Review of Psychology, 53, 401–433.CrossRefGoogle Scholar