Electrical stimulation of the medial orbitofrontal cortex in humans elicits pleasant olfactory perceptions

Abstract

Background: Olfactory hallucinations can be part of epileptic seizures of orbitofrontal origin. Olfactory hallucinations, however, are rare and therefore the semiology, localization and lateralization characteristics are underdetermined. In addition, many discrepancies are found in the literature regarding olfactory processing and orbitofrontal (OF) functions and olfactory function. Particularly, the questions of laterality and affective component in coding of odors in the OF cortex remain controversial. Aims: This study explored whether cortical electrical stimulation of the OF and mesiotemporal brain can trigger olfactory hallucinations with special focus on olfactory percepts in terms of laterality and hedonics. Materials and methods: Eight patients with temporal lobe epilepsy participated in the study, at the time of invasive exploration of their epilepsy. The most distal contact of the OF and anterior hippocampus depth electrodes were stimulated (50 Hz, 0.2 ms biphasic pulse; maximal stimulation 4 mA). Patients were instructed to report any kind of sensation they might experience. Intracranial depth electrodes were localized (iElectrodes): subject-specific brain mask, subcortical segmentation and cortical parcellation based on the Destrieux atlas (FreeSurfer) were superposed to the coregistered T1-weighted MRI and CT images (SPM). The center of mass of each electrode-artifact cluster determined the electrode localization. The electrode labeling was done in patient space. To obtain the electrode coordinates in Montreal Neurological Institute (MNI) space, the images obtained previously in the patient space were first segmented and normalized (SPM). Then, the localization procedure (iElectrodes) was run again with these new normalized images in MNI space. Results: No hallucination was evoked by stimulation, neither of the right nor the left hippocampus (8/8 patients). Pleasant olfactory hallucinations were evoked by OF stimulation in 5/8 patients in either hemisphere. Patients named the percept as the smell of lemon or coffee for example. Among those 5 patients, electrodes were localized in the cortex of the olfactory sulcus, medial orbital sulcus or medial OF gyrus. Increasing stimulation amplitude changed the olfactory percept identification in 3 out of those 5 patients. No affective judgement or change in perceived odor intensity was reported by the patients. No hallucination was evoked by the stimulation of the white matter of the medial OF brain in 3/8 patients independently of the hemisphere stimulated. Conclusions: This study demonstrated that stimulation of the cortex of the medial OF brain and not of its white matter elicits specific pleasant olfactory hallucinations independently of the hemisphere stimulated, supporting one symmetrical olfactory processing in human.

The human olfactory bulb processes odor valence representation and cues motor avoidance behavior

“…However, a recent study on human participants demonstrated that, akin to rodents, pleasant but not negative odors are preferentially processed in the olfactory tubercle ( 59 ). Moreover, intracranial electric stimulation of the OFC, an area previously linked to odor valence processing in humans, could only produce pleasant odor experiences ( 60 ). This separation between valence extremes support the 2D valence hypothesis postulating that odor valence perception is not represented by a unidimensional spectrum, ranging from unpleasant to pleasant.…”

The human olfactory bulb process odor valence representation and initiate motor avoidance behavior

“…Whether this regional-specific valence separation in processing also occurs in humans is not known. However, a recent study demonstrated that intracranial electric stimulation of the OFC, an area previously linked to odor valence processing in humans, could only produce pleasant odor experiences (Bérard et al 2020). The separation demonstrated in rodents does, however, support the 2-dimensional valence hypothesis that odor valence perception is not represented by a unidimensional spectrum, ranging from unpleasant to pleasant.…”

A structural MRI study of global developmental delay in infants (<2 years old)

“…To ensure the quality of skull dissection and the accuracy of gray matter/white matter boundary segmentation, the results of skull dissection and brain tissue segmentation were examined by two skilled anatomical operators. After the cortical reconstruction was completed, the left and right hemispheres were divided into 33 brain regions according to the FreeSurfer cortical atlas ( 15 ), and the average CT and the summed SA of each brain region were calculated. Linear mixed effect (LME) ( 16 ) models were used to model the development trajectory, and three models (linear, quadratic, and logistic curve) were used to fit the trajectory.…”