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October 16, 2018; 91 (16) Article

Changes in subjective experience elicited by direct stimulation of the human orbitofrontal cortex

Kieran C. R. Fox, Jennifer Yih, Omri Raccah, Shrita L. Pendekanti, Lauren E. Limbach, Daniella D. Maydan, Josef Parvizi
First published September 19, 2018, DOI: https://doi.org/10.1212/WNL.0000000000006358
Kieran C. R. Fox
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Jennifer Yih
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Omri Raccah
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Shrita L. Pendekanti
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Lauren E. Limbach
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Daniella D. Maydan
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Josef Parvizi
From the Department of Neurology and Neurological Sciences, Stanford University, CA.
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Changes in subjective experience elicited by direct stimulation of the human orbitofrontal cortex
Kieran C. R. Fox, Jennifer Yih, Omri Raccah, Shrita L. Pendekanti, Lauren E. Limbach, Daniella D. Maydan, Josef Parvizi
Neurology Oct 2018, 91 (16) e1519-e1527; DOI: 10.1212/WNL.0000000000006358

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Abstract

Objective We applied direct cortical stimulation (DCS) to the orbitofrontal cortex (OFC) in neurosurgical patients implanted with intracranial electrodes to probe, with high anatomic precision, the causal link between the OFC and human subjective experience.

Methods We administered 272 instances of DCS at 172 OFC sites in 22 patients with intractable focal epilepsy (from 2011 to 2017), none of whom had seizures originating from the OFC.

Results Our observations revealed a rich variety of affective, olfactory, gustatory, and somatosensory changes in the subjective domain. Elicited experiences were largely neutral or negatively valenced (e.g., aversive smells and tastes, sadness, and anger). Evidence was found for preferential left lateralization of negatively valenced experiences and strong right lateralization of neutral effects. Moreover, most of the elicited effects were observed after stimulation of OFC tissue around the transverse orbital sulcus, and none were seen in the most anterior aspects of the OFC.

Conclusions Our study yielded 3 central findings: first, a dissociation between the “silent” anterior and nonsilent middle/posterior OFC where stimulation clearly elicits changes in subjective experience; second, evidence that the OFC might play a causal role in integrating affect and multimodal sensory experiences; and third, clear evidence for left lateralization of negatively valenced effects. Our findings provide important information for clinicians treating OFC injury or planning OFC resection and scientists seeking to understand the brain basis for the integration of sensation, cognition, and affect.

Glossary

DCS=
direct cortical stimulation;
OFC=
orbitofrontal cortex;
MNI=
Montreal Neurological Institute

Footnotes

  • ↵* These authors contributed equally to this work.

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • CME Course: NPub.org/cmelist

  • Received February 8, 2018.
  • Accepted in final form July 13, 2018.
  • © 2018 American Academy of Neurology
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