Abstract
It has long been recognized that olfaction and emotion are linked. While chemosensory research using both human and rodent models have indicated a change in emotion can contribute to olfactory dysfunction, there are few studies addressing the contribution of olfaction to a modulation in emotion. In mice, olfactory deficits have been linked with heightened anxiety levels, suggesting that there could be an inverse relationship between olfaction and anxiety. Furthermore, increased anxiety is often co-morbid with psychiatric conditions such as attention disorders. Our study aimed to investigate the roles of olfaction in modulating anxiety. Voltage-gated potassium ion channel Kv1.3 knockout mice (Kv1.3−/−), which have heightened olfaction, and wild-type (WT) mice were examined for anxiety-like behaviors using marble burying (MB), light-dark box (LDB) and elevated-plus maze (EPM) tests. Because Kv1.3−/− mice have increased locomotor activity, inattentive and hyperactive behaviors were quantified for both genotypes. Kv1.3−/− mice showed increased anxiety levels compared to their WT counterparts and administration of methylphenidate (MPH) via oral gavage alleviated their increased anxiety. Object-based attention testing indicated young and older Kv1.3−/− mice had attention deficits and treatment with MPH also ameliorated this condition. Locomotor testing through use of a metabolic chamber indicated that Kv1.3−/− mice were not significantly hyperactive and MPH treatment failed to modify this activity. Our data suggest that heightened olfaction does not necessarily lead to decreased anxiety levels, and that Kv1.3−/− mice may have behaviors associated with inattentiveness.
Highlights
Olfaction is phylogenetically the most ancient sense and has a close association with emotion; it has been well studied that the perception of an odor cue can be altered depending upon reward, threat, or homeostatic state (Hamann, 2003; Krusemark et al, 2013; Nunez-Parra et al, 2014)
While these metrics implicated an increased anxiety level in the Kv1.3−/− mice, there was not a significant difference in exploratory behavior as assessed by total number of transitions between boxes (Figure 1F; 2-way analysis of variance (ANOVA), sex: p = 0.057; genotype: p = 0.138; interaction: p = 0.382) there was a trend that the Kv1.3−/− moved less in this assay and for that of females
While younger Kv1.3−/− mice trended to exhibit reduced attention to an object-based attention task, older Kv1.3−/− mice performed with a significant deficit, which was ameliorated by MPH treatment
Summary
Olfaction is phylogenetically the most ancient sense and has a close association with emotion; it has been well studied that the perception of an odor cue can be altered depending upon reward, threat, or homeostatic state (Hamann, 2003; Krusemark et al, 2013; Nunez-Parra et al, 2014). Anxiety and Attention in Kv1.3-Null Mice function can be disturbed via disease or nutritional state (Rugarli, 1999; Aimé et al, 2007; Thiebaud et al, 2014), olfactory function can be altered experimentally through surgical (Meredith et al, 1983) or chemical lesions (Slotnick et al, 2007; DiBenedictis et al, 2014), or via genetic engineering (Fadool et al, 2004; Glinka et al, 2012). Surgical removal of the olfactory bulb (OB) is classically known to result in anxiety- and depression-like behaviors (for review see Brunjes, 1992). Olfactory bulbectomy models have frequently been used to screen for antidepressant drugs (Cairncross et al, 1977; Kelly et al, 1997; Song and Leonard, 2005)
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