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Influences of temporal lobe epilepsy and temporal lobe resection on olfaction

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Abstract

Although temporal lobe epilepsy (TLE) and resection (TLR) impact olfactory eloquent brain structures, their influences on olfaction remain enigmatic. We sought to more definitively assess the influences of TLE and TLR on olfaction using three well-validated olfactory tests and measuring  the tests’ associations with the volume of numerous temporal lobe brain structures. The University of Pennsylvania Smell Identification Test and an odor detection threshold test were administered to 71 TLE patients and 71 age- and sex-matched controls; 69 TLE patients and controls received an odor discrimination/memory test. Fifty-seven patients and 57 controls were tested on odor identification and threshold before and after TLR; 27 patients and 27 controls were similarly tested for odor detection/discrimination. Scores were compared using analysis of variance and correlated with pre- and post-operative volumes of the target brain structures. TLE was associated with bilateral deficits in all test measures. TLR further decreased function on the side ipsilateral to resection. The hippocampus and other structures were smaller on the focus side of the TLE subjects. Although post-operative volumetric decreases were evident in most measured brain structures, modest contralateral volumetric increases were observed in some cases. No meaningful correlations were evident pre- or post-operatively between the olfactory test scores and the structural volumes. In conclusion, we demonstrate that smell dysfunction is clearly a key element of both TLE and TLR, impacting odor identification, detection, and discrimination/memory. Whether our novel finding of significant post-operative increases in the volume of brain structures contralateral to the resection side reflects plasticity and compensatory processes requires further study.

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Acknowledgements

We thank the following individuals for their contributions to this project: David Adelman, Ritvijj Bowry, Charles Glass, Ruben Gur, Mark Korczykowski, Laurie Loevner, Dawn Mechanic-Hamilton, Helen Li, David L. Minkoff, Jessica Morton, Veena Narayan, Michael O’Connor, Kiana Owzar, David Roalf, Muhammad Shah, Joseph Tracy, John Treem, Steven E. West, and Paul A. Yushkevich. Marilyn Jones-Gotman provided comments on the final draft.

Funding

Supported by NIH Grant RO1 DC04278 awarded to RLD.

Author information

Authors and Affiliations

  1. Smell and Taste Center, Perelman School of Medicine, Hospital of the University of Pennsylvania, 5 Ravdin Pavilion, 3400 Spruce Street, Philadelphia, PA, 19104-4283, USA

    Richard L. Doty, Isabelle Tourbier, Jessica K. Neff, Jonathan Silas, Bruce Turetsky, Paul Moberg, Taehoon Kim, Natasha Mirza & Anthony Risser

  2. Department of Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    John Pluta & John A. Detre

  3. Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Taehoon Kim, Gordon Baltuch & John A. Detre

  4. Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Gordon Baltuch

  5. Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Bruce Turetsky & Paul Moberg

  6. Department of Otorhinolaryngology, Head and Neck Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Richard L. Doty, Isabelle Tourbier, Jessica K. Neff & Natasha Mirza

  7. Department of Neurology, New York University Langone Medical Center, New York, NY, 10016, USA

    Jaqueline French

  8. Department of Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, PA, USA

    Ashwini D. Sharan

  9. Department of Neurology, Thomas Jefferson University Hospital, Philadelphia, PA, USA

    Michael J. Sperling

  10. Department of Psychology, Middlesex University, London, UK

    Jonathan Silas

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  1. Richard L. Doty
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  2. Isabelle Tourbier
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  12. Natasha Mirza
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  14. Gordon Baltuch
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  15. John A. Detre
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Corresponding author

Correspondence to Richard L. Doty.

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Conflicts of interest

RLD is President and major shareholder of Sensonics International, the company that manufactures and distributes olfactory and gustatory tests, including the commercial version of the University of Pennsylvania Smell Identification Test (UPSIT) used in this study. The remaining authors report no potential conflicts with commercial relationships of direct relevance to the current research.

Ethical standards

The study was approved by the University of Pennsylvania’s Office of Regulatory Affairs. The study was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All participants were paid $20/hour for their time.

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Informed written consent was obtained from all participants.

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Doty, R.L., Tourbier, I., Neff, J.K. et al. Influences of temporal lobe epilepsy and temporal lobe resection on olfaction. J Neurol 265, 1654–1665 (2018). https://doi.org/10.1007/s00415-018-8891-y

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  • DOI: https://doi.org/10.1007/s00415-018-8891-y

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