Disinhibition of olfaction: Human olfactory performance improves following low levels of alcohol

Highlights

• We test olfactory performance after ingestion of alcohol.

• We find that low levels of alcohol improve olfactory performance.

• We hypothesize that true human olfactory abilities are obscured by cortical inhibition.

Abstract

We hypothesize that true human olfactory abilities are obscured by cortical inhibition. Alcohol reduces inhibition. We therefore tested the hypothesis that olfactory abilities will improve following alcohol consumption. We measured olfaction in 85 subjects, 45 in a between-subjects design, and 40 in a repeated-measures within-subjects design before and after consumption of alcoholic or non-alcoholic beverages. Subjects were also assessed using neurocognitive measures of inhibition. Following alcohol consumption, blood alcohol levels ranged from 0.005% to 0.11%. Across subjects, before any consumption of alcohol, we found that individuals who were less inhibited had lower (better) olfactory detection thresholds (r = 0.68, p < 0.005). Moreover, after alcohol consumption, subjects with low alcohol levels could make olfactory discriminations that subjects with 0% alcohol could not make (chance = 33%, alcohol = 51.3 ± 22.7%, control = 34.7 ± 31.6%, t(43) = 2.03, p < 0.05). Within subjects, we found correlations between levels of alcohol and olfactory detection (r = 0.63, p < 0.005) and discrimination (r = −0.50, p < 0.05), such that performance was improved at low levels of alcohol (significantly better than baseline for detection) and deteriorated at higher levels of alcohol. Finally, levels of alcohol-induced improved olfactory discrimination were correlated with levels of alcohol-induced cognitive disinhibition (r = 0.48, p < 0.05). Although we cannot rule out alternative non-inhibitory alcohol-induced routes of influence, we conclude that improved olfaction at low levels of alcohol supports the notion of an inhibitory mechanism obscuring true olfactory abilities.

Introduction

Although humans direct only limited attention to olfaction [1], [2], human olfactory abilities are high [3], [4], [5], [6]. Consistent with this dissociation, humans are very poor at assessing their own olfactory abilities [7], [8]. Moreover, these abilities can improve with practice. For example, through aversive conditioning humans can learn to discriminate previously indiscriminable odors [9], through practice humans can learn to track a scent trail [10], and repeated exposure to an odorant can lower (improve) its detection threshold [11], in some cases driving a shift from complete lack of detection to clear detectability [12], [13]. Whereas these examples entail gradual changes in olfactory abilities, there are other examples of instantaneous improvements in olfaction. Many of these cases are anecdotal. For example, in his story “The Dog Beneath The Skin” [14]. Oliver Sacks describes a medical student whose sense of smell became extremely sensitive after a discrete instance of recreational drug use. This is not the only report of rapid-onset hyper-olfaction. In a separate case, following stroke, a 65 year-old man shifted to olfactory exploration as his primary mode of object investigation, and tended toward better spontaneous odor naming in comparison to healthy controls [15]. Whereas the influence of training and conditioning may be attributable to plasticity anywhere in the olfactory system [16], and the influence of drugs may reflect peripheral mechanisms such as cannabinoid effects on CB1-receptors in the olfactory bulb [17], [18], rapid-onset hyper-olfaction following stroke implies the unveiling of olfactory capabilities that were previously masked or inhibited. With this in mind, the working hypothesis of this study is that human olfaction is under constant inhibition.

The ventral temporal brain structures that contain primary olfactory cortex [19] are under inhibitory influence of the prefrontal cortex (PFC) [20], [21]. One path toward reducing this inhibition is alcohol consumption [22], [23]. Alcohol consumption drives behavioral effects similar to those seen following PFC lesions, including deficits in planning, information processing, attention, and inhibitory control [24], [25], [26], [27], the latter evident even after only moderate doses of alcohol alone [24], [28].

Previous studies examining the effects of alcohol consumption on olfaction came to mixed conclusions. In agreement with our hypothesis, one early study found that moderate doses of alcohol increased sensitivity to the odorant guaiacol (a smoky odor) [29]. This, however, was a between-subjects design, susceptible to non-alcohol related group differences. In contrast, other studies using within subject designs reported either declined [30], [31], [32], or unchanged [31] olfactory performance following alcohol consumption. Here we set out to test the hypothesis that alcohol may improve olfactory performance in three separate experimental designs. In Experiments 1 and 2 we used a within-subjects repeated experimental design in a highly controlled laboratory setting where we measured olfactory performance as well as non-olfactory measures of inhibition on separate days before and after consumption of a beverage that was either with or without alcohol. Experiment 3 was a field-experiment where we measured olfactory performance and levels of alcohol amongst pub-goers. These experiments converged to imply that whereas high doses of alcohol impair olfactory performance, low doses of alcohol lead to improvements in olfactory performance above the no-alcohol baseline. These improvements are consistent with our hypothesis regarding inhibition in human olfaction.