Olfactory hallucinations elicited by electrical stimulation via subdural electrodes: effects of direct stimulation of olfactory bulb and tract.

Gogi Kumar, Csaba Juhász, Sandeep Sood, Eishi Asano
Author Information
  1. Gogi Kumar: Department of Pediatrics, Wayne State University, Detroit Medical Center, Detroit, MI 48201, USA.

Abstract

In 1954, Penfield and Jasper briefly described that percepts of unpleasant odor were elicited by intraoperative electrical stimulation of the olfactory bulb in patients with epilepsy. Since then, few peer-reviewed studies have reported such phenomena elicited by stimulation mapping via subdural electrodes implanted on the ventral surface of the frontal lobe. Here, we determined what types of olfactory hallucinations could be reproduced by such stimulation in children with focal epilepsy. This study included 16 children (age range: 5 to 17 years) who underwent implantation of subdural electrodes to localize the presumed epileptogenic zone and eloquent areas. Pairs of electrodes were electrically stimulated, and clinical responses were observed. In case a patient reported a perception, she/he was asked to describe its nature. We also described the stimulus parameters to elicit a given symptom. Eleven patients reported a perception of smell in response to electrical stimulation while the remaining five did not. Nine patients perceived an unpleasant smell (like bitterness, smoke, or garbage) while two perceived a pleasant smell (like strawberry or good food). Such olfactory hallucinations were induced by stimulation proximal to the olfactory bulb or tract on either hemisphere but not by that of orbitofrontal gyri lateral to the medial orbital sulci. The range of stimulus parameters employed to elicit olfactory hallucinations was comparable to those for other sensorimotor symptoms. Our systematic study of children with epilepsy replicated stimulation-induced olfactory hallucinations. We failed to provide evidence that a positive olfactory perception could be elicited by conventional stimulation of secondary olfactory cortex alone.

References

  1. Clin Neurophysiol. 2011 Oct;122(10):1929-42 [PMID: 21498109]
  2. Neurosurgery. 1999 Nov;45(5):1186-91 [PMID: 10549936]
  3. Epilepsy Res. 2009 Nov;87(1):77-87 [PMID: 19734012]
  4. Epilepsia. 2002 Dec;43(12):1543-50 [PMID: 12460257]
  5. J Neurosci. 1994 Sep;14(9):5437-52 [PMID: 8083747]
  6. Brain. 1991 Feb;114 ( Pt 1A):71-84 [PMID: 1998891]
  7. Brain Res Brain Res Rev. 2005 Dec 15;50(2):287-304 [PMID: 16213593]
  8. J Neurosci Methods. 2008 Sep 15;174(1):106-15 [PMID: 18657573]
  9. Ann Neurol. 1982 Aug;12(2):129-44 [PMID: 7125603]
  10. J Neurosci Methods. 2007 May 15;162(1-2):303-8 [PMID: 17343918]
  11. Neuro Endocrinol Lett. 2002 Apr;23(2):79-84 [PMID: 12011790]
  12. Expert Rev Med Devices. 2007 Sep;4(5):623-31 [PMID: 17850197]
  13. Arch Otolaryngol. 1982 Feb;108(2):90-2 [PMID: 7059319]
  14. Epilepsy Res. 2007 Sep;76(2-3):131-9 [PMID: 17723289]
  15. Neuron. 2000 Jun;26(3):735-45 [PMID: 10896168]
  16. Clin Neurophysiol. 2012 Oct;123(10):1917-24 [PMID: 22503906]
  17. Epilepsia. 2010 Apr;51(4):573-82 [PMID: 19845730]
  18. Brain Cogn. 1993 Jul;22(2):182-98 [PMID: 8373572]
  19. Brain. 2002 Jan;125(Pt 1):86-101 [PMID: 11834595]
  20. Neuron. 2005 Nov 3;48(3):417-30 [PMID: 16269360]
  21. Arch Otolaryngol Head Neck Surg. 1987 Sep;113(9):933-5 [PMID: 3606843]
  22. Epilepsia. 1995 Jun;36(6):531-42 [PMID: 7555965]
  23. Neurology. 2004 Sep 14;63(5):858-64 [PMID: 15365137]
  24. Neuron. 2005 Nov 3;48(3):431-54 [PMID: 16269361]
  25. Brain. 1993 Apr;116 ( Pt 2):397-414 [PMID: 8461973]
  26. Percept Mot Skills. 2000 Dec;91(3 Pt 1):771-81 [PMID: 11153847]
  27. Brain. 2009 Apr;132(Pt 4):1038-47 [PMID: 19286694]
  28. J Neurol Neurosurg Psychiatry. 2009 Jun;80(6):686-8 [PMID: 19448096]
  29. Int J Biomed Imaging. 2007;2007:13963 [PMID: 17710251]

Grants

  1. NS47550/NINDS NIH HHS
  2. K23 NS047550/NINDS NIH HHS
  3. NS64033/NINDS NIH HHS
  4. R01 NS064033-05/NINDS NIH HHS
  5. R01 NS064033/NINDS NIH HHS
  6. K23 NS047550-05/NINDS NIH HHS

MeSH Term

Adolescent
Child
Child, Preschool
Electric Stimulation
Electrodes, Implanted
Electroencephalography
Epilepsy
Female
Frontal Lobe
Hallucinations
Humans
Magnetic Resonance Imaging
Male
Neurosurgical Procedures
Olfactory Bulb
Olfactory Pathways
Smell
Subdural Space

Word Cloud

Created with Highcharts 10.0.0olfactorystimulationhallucinationselicitedelectricalbulbpatientsepilepsyreportedsubduralelectrodeschildrenperceptionsmelldescribedunpleasantviastudystimulusparameterselicitperceivedliketract1954PenfieldJasperbrieflyperceptsodorintraoperativeSincepeer-reviewedstudiesphenomenamappingimplantedventralsurfacefrontallobedeterminedtypesreproducedfocalincluded16agerange:517yearsunderwentimplantationlocalizepresumedepileptogeniczoneeloquentareasPairselectricallystimulatedclinicalresponsesobservedcasepatientshe/heaskeddescribenaturealsogivensymptomElevenresponseremainingfiveNinebitternesssmokegarbagetwopleasantstrawberrygoodfoodinducedproximaleitherhemisphereorbitofrontalgyrilateralmedialorbitalsulcirangeemployedcomparablesensorimotorsymptomssystematicreplicatedstimulation-inducedfailedprovideevidencepositiveconventionalsecondarycortexaloneOlfactoryelectrodes:effectsdirect

Similar Articles

Cited By