Abstract
Event-related potentials (ERPs) were recorded in response to mildly aversive somatosensory and auditory stimuli. Patients with orbitofrontal lesions exhibited enhanced ERPs (i.e., P3 amplitudes), as compared with control subjects. Moreover, these patients did not habituate to somatosensory stimuli across blocks of trials. The results were specific to orbitofrontal damage, since patients with damage to the dorsolateral prefrontal cortex did not exhibit enhanced P3 amplitudes. These findings suggest that damage to the orbitofrontal cortex impairs the ability to modulate or inhibit neural responses to aversive stimuli. The findings are couched in terms of dynamic filtering theory, which suggests that the orbitofrontal cortex is involved in the selection and active inhibition of neural circuits associated with emotional responses.
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Baldo, J. V., & Shimamura, A. P. (2000). Spatial and color working memory in patients with lateral prefrontal cortex lesions. Psychobiology, 28, 156–167.
Bechara, A., Damasio, H., & Damasio, A. R. (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex, 10, 295–307.
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.
Butter, C. M. (1964). Habituation of responses to novel stimuli in monkeys with selective frontal lesions. Science, 144, 313–315.
Butter, C. M., McDonald, J. A., & Snyder, D. R. (1969). Orality, preference behavior, and reinforcement value of nonfood objects in monkeys with orbital frontal lesions. Science, 164, 1306–1307.
Chao, L. L., & Knight, R. T. (1996). Prefrontal and posterior cortical activation during auditory working memory. Cognitive Brain Research, 4, 27–37.
Damasio, A. R. (1998). The somatic marker hypothesis and the possible functions of the prefrontal cortex. In A. C. Roberts, T. W. Robbins, & L. Weiskrantz (Eds.), The prefrontal cortex: Executive and cognitive function (pp. 103–116). Oxford: Oxford University Press.
Damasio, A. R., Tranel, D., & Damasio, H. (1990). Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behavioural Brain Research, 41, 81–94.
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural circuitry of emotion regulation: A possible prelude to violence. Science, 289, 591–594.
D’Esposito, M., Postle, B. R., Ballard, D., & Lease, J. (1999). Maintenance versus manipulation of information held in working memory: An event-related fMRI study. Brain & Cognition, 41, 66–86.
Dias, R., Robbins, T. W., & Roberts, A. C. (1996). Dissociation in prefrontal cortex of affective and attentional shifts. Nature, 380, 69–72.
Harlow, J. M. (1848). Passage of an iron rod through the head. Boston Medical & Surgical Journal, 39, 389–393.
Harlow, J. M. (1868). Recovery of an iron rod through the head. Publications of the Massachusetts Medical Society, 2, 327–347.
Hartikainen, K., Ogawa, K. H., Soltani, M., Pepitone, M., & Knight, R. T. (2000). Altered emotional influence on visual attention subsequent to orbitofrontal damage in humans. Society for Neuroscience Abstracts, 26, 2023.
Iversen, S. D., & Mishkin, M. (1970). Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Experimental Brain Research, 11, 376–386.
Kaipio, M.-L., Alho, K., Winkler, I., Escera, C., Surma-Aho, O., & Näätänen, R. (1999). Event-related brain potentials reveal covert distractibility in closed head injuries. NeuroReport, 10, 2125–2159.
Knight, R. T. (1984). Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalography & Clinical Neurophysiology, 59, 9–20.
Knight, R. T. (1996). Contribution of human hippocampal region to novelty detection. Nature, 383, 256–259.
Knight, R. T., Scabini, D., Woods, D. L., & Clayworth, C. C. (1989). Contributions of temporal-parietal junction to the human auditory P3. Brain Research, 502, 109–616.
Knight, R. T., Staines, W. R., Swick, D., & Chao, L. L. (1999). Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychologica, 101, 159–178.
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184.
Macmillan, M. (1986). A wonderful journey through skull and brains: The travels of Mr. Gage’s tamping iron. Brain & Cognition, 5, 67–107.
Macmillan, M. (1999). An odd kind of fame: Stories of Phineas Gage. Cambridge, MA: MIT Press, Bradford Books.
Mattson, A. J., & Levin, H. S. (1990). Frontal lobe dysfunction following closed head injury. Journal of Nervous & Mental Disease, 178, 282–291.
McGaugh, J. L. (2000). Memory: A century of consolidation. Science, 287, 248–251.
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.
Opitz, B., Mecklinger, A., Friederici, A. D., & von Cramon, D. Y. (1999). The functional neuroanatomy of novelty processing: Integrating ERP and fMRI results. Cerebral Cortex, 9, 379–391.
Panksepp, J. (1998). Affective neuroscience: The foundations of human and animal emotions. New York: Oxford University Press.
Petrides, M. (1998). Specialized systems for the processing of mnemonic information within the primate frontal cortex. In A. C. Roberts, T. W. Robbins, & L. Weiskrantz (Eds.), The prefrontal cortex: Executive and cognitive function (pp. 103–116). Oxford: Oxford University Press.
Petrides, M., & Pandya, D. N. (1994). Comparative architectonic analysis of the human and the macaque frontal cortex. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (Vol. 9, pp. 17–58). Amsterdam: Elsevier.
Puce, A., Constable, R. T., Luby, M. L., McCarthy, G., Nobre, A. C., Spencer, D. D., Gore, J. C., & Allison, T. (1995). Functional magnetic resonance imaging of sensory and motor cortex: Comparison with electrophysiological localization. Journal of Neurosurgery, 83, 262–270.
Roberts, N. A., Levens, S. M., McCoy, K., Werner, K., Beer, J. S., Scabini, D., & Knight, R. T. (2001). Orbitofrontal cortex and activation of defensive responses. Society for Neuroscience Abstracts, 27, 1705.
Rolls, E. T. (2000). The orbitofrontal cortex and reward. Cerebral Cortex, 10, 284–294.
Rolls, E. T., Hornak, J., Wade, D., & McGrath, J. (1994). Emotionrelated learning in patients with social and emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery & Psychiatry, 57, 1518–1524.
Shallice, T., & Burgess, P. (1993). Supervisory control of action and thought selection. In A. Baddeley & L. Weiskrantz (Eds.), Attention: Selection, awareness, and control: A tribute to Donald Broadbent (pp. 171–187). New York: Oxford University Press, Clarendon Press.
Shimamura, A. P. (2000). The role of the prefrontal cortex in dynamic filtering. Psychobiology, 28, 207–218.
Shimamura, A. P. (in press). Muybridge in motion: Travels in art, psychology, and neurology. History of Photography. Smith, E. E., & Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science, 283, 1657–1661.
Solbakk, A. K., Reinvang, I., Nielsen, C., & Sundet, K. (1999). ERP indicators of disturbed attention in mild closed head injury: A frontal lobe syndrome? Psychophysiology, 36, 802–817.
Soltani, M., & Knight, R.T. (in press). Neural origins of the P300. Critical Reviews in Neurobiology.
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This research was supported by NIH Grants DA14110 to A.P.S. and NS21135 to R.T.K. and by funding from the Veterans Administration Research Service.
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Rule, R.R., Shimamura, A.P. & Knight, R.T. Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cognitive, Affective, & Behavioral Neuroscience 2, 264–270 (2002). https://doi.org/10.3758/CABN.2.3.264
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DOI: https://doi.org/10.3758/CABN.2.3.264