Pervasive olfactory impairment after bilateral limbic system destruction

Abstract

What pattern of brain damage could completely obliterate the sense of olfaction in humans? We had an opportunity to address this intriguing question in Patient B., who has extensive bilateral damage to most of the limbic system, including the medial and lateral temporal lobes, orbital frontal cortex, insular cortex, anterior cingulate cortex, and basal forebrain, caused by herpes simplex encephalitis. The patient demonstrated profound impairments in odor identification and recognition. Moreover, he could not discriminate between olfactory stimuli, and he had severe impairments in odor detection. Reliable stimulus detection was obtained only for solutions of the organic solvent acetone and highly concentrated solutions of ethanol. In contrast to the more circumscribed olfactory deficits demonstrated in patients with damage confined to either the temporal lobes or orbitofrontal cortex (which tend to involve odor identification but not odor detection), Patient B. demonstrated a strikingly severe and complete anosmia. This contrast in olfactory abilities and deficits as a result of different anatomical pathology affords new insights into the neural substrates of olfactory processing in humans.

Keywords:

• Smell
• Olfaction
• Lesion method
• Herpes simplex encephalitis
• Limbic system

Acknowledgments

Supported by National Institute on Drug Abuse (NIDA) R01 DA022549 and National Institute of Neurological Disorders and Stroke (NINDS) P50 NS19632 (D.T.). We thank Ken Manzel for assistance with data collection and analysis and for help in preparing the manuscript, and Marilyn Dolezal for help preparing the references.

Notes

¹In this context, it is interesting to note that B. did not evidence “urges” or “cravings” to smoke following his lesion onset, which is consistent with the idea that insula damage (which B. had in entirety in both left and right hemispheres) can disrupt smoking addiction by abolishing urges and cravings for nicotine (Naqvi, Rudrauf, Damasio, & Bechara, 2007).

²For a response to be scored as an “accurate identification” when the correct name was not provided, the participant had to generate a specific description that unambiguously identified the smell; see H. Damasio, Tranel, Grabowski, Adolphs, and Damasio (2004) for a complete description of this scoring method.

³Unfortunately, we do not have a postmortem study of B.'s brain, out of respect for his family's wishes.