Research report
Monorhinal odor identification and depression scores in patients with seasonal affective disorder

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Abstract

Background: Visual and olfactory pathways are interconnected. Olfactory deafferentation unmasks photoperiodic responsiveness in some nonphotoperiodic animals such as laboratory rats. By analogy, we hypothesized that olfactory deficits may unmask seasonal rhythms in certain individuals, namely those with seasonal affective disorder (SAD). Since previous studies suggest lateralized hemispheric dysfunction in SAD, and since olfactory neurons’ primary projections are largely ipsilateral, we assessed olfactory identification performance on both the right and left side of the nose. Methods: Twenty-four patients with SAD and 24 matched controls were studied using a phenyl ethyl alcohol detection threshold test bilaterally and the University of Pennsylvania Smell Identification Test unilaterally. Subjects rated their mood using the Self Assessment Mood Scale for SAD. Patients’ testing was done in both ‘depressed’ and ‘improved on light’ states. Results: No difference in olfactory performance was found between patients and controls or between patients before and after light treatment. However, right-side identification scores were negatively correlated with ‘typical’ depression scores (r=−0.56, P=0.006), while left-side olfactory scores were not. Atypical depression scores were unrelated to olfactory performance. Similar correlations emerged between the olfactory identification laterality quotient (Right−Left)/(Right+Left) and typical depressive scores (r=−0.64, P<0.001) and total depression scores (r=−0.59, P<0.004). Limitations: We studied a demographically heterogeneous sample and did not control for menstrual factors. Discussion: Our results add to previous evidence of lateralized hemispheric involvement in SAD and suggest that olfaction may be related to seasonal emotional rhythms in humans.

Introduction

It is often assumed that the human sense of smell is incapable of mediating numerous communicative functions subserved by olfaction in many other animals. Recently, however, it has been suggested that humans may influence each other’s biological rhythms via body odors (Stern and McClintock 1998).

Since neuronal connections between main olfactory pathways and limbic structures persist in humans, olfactory functioning has been a logical focus of investigation in neuropsychiatric disorders, with consistent abnormal findings in schizophrenia, Alzheimer disease and Parkinson disease Doty, 1991, Martzke et al., 1997. In depression, however, the results of olfactory testing have been mixed. No olfactory deficits were reported in some studies of non-seasonal depression Warner et al., 1990, Amsterdam et al., 1987 and seasonal depression (Oren et al., 1995), while other studies found an abnormal olfactory identification ability in nonseasonally depressed patients Serby et al., 1990, Rupp et al., 1997.

Right-posterior hemispheric abnormalities have been suggested by neuropsychological testing in patients with seasonal affective disorder (SAD) O’Brien et al., 1993, Michalon et al., 1997 and evidence of decreased left prefrontal and right-posterior activation has been found in an electrophysiological study on SAD (Allen et al., 1993). Anatomically, the olfactory system is unique among other sensory systems because of predominantly ipsilateral projections (Furukawa et al., 1988). In this study we therefore employ, for the first time in mood disorders, monorhinal odor identification testing Doty et al., 1989, Doty et al., 1992.

Olfactory circuitry has been associated with both depression and photoperiodic responses in animal studies. Indeed, the olfactory bulbectomized rat has been used as an animal model for depression (Brunjes 1992). In nonphotoperiodic animals such as rats, olfactory deafferentation unmasks photoperiodic responsiveness Nelson and Zucker, 1981, Nelson et al., 1985. In contrast, in photoperiodic animals, such as hamsters, golden-mantled ground squirrels, and the lesser mouth lemur (a photoperiodic primate), olfactory bulbectomy interferes with some of the effects of photoperiodic changes Miro et al., 1980, Ruby et al., 1993, Schilling and Perret, 1993.

Although light treatment is an effective antidepressant for patients with SAD Terman et al., 1998, Eastman et al., 1998, mood improvement after light treatment is smaller than the spontaneous improvement during summer (Postolache et al., 1998). A number of physical, chemical, biological, and socio-economic variables may account for this difference, among them, olfactory factors, given the contribution of the sense of smell to seasonal rhythms in other mammals. As the neurocircuitry responsible for seasonal changes exists latently in nonphotoperiodic animals and can be activated by lesioning olfactory pathways Nelson and Zucker, 1981, Nelson et al., 1985, we speculated that olfactory deficits may be associated with latent seasonal rhythms becoming manifest in vulnerable human individuals, namely in patients with SAD. The modulatory effect of olfaction on seasonal rhythms could be mediated via complex connections between visual and olfactory pathways, specifically convergent retinal and olfactory projections in the cortical region of the medial amygdala and lateral hypothalamus Cooper et al., 1994, Leak and Moore, 1997.

We hypothesized that olfactory performance deficits would be found in untreated depressive SAD patients, that light treatment would improve olfactory performance in patients with SAD, that the olfactory performance would correlate with the depressive scores, and that the relationship between olfactory performance and depressive scores would be lateralized.

Section snippets

Subjects and mood ratings

We studied 24 patients and 24 matched controls (Table 1), after obtaining informed consent. The protocol was approved by the Institutional Review Board of the intramural NIMH. Patients met Rosenthal criteria for SAD (Rosenthal et al., 1984) and DSM-IV criteria for a past major depressive episode. Patients with other axis I psychiatric diagnosis, current smokers, those medically ill, or with history of allergy to cosmetics, were excluded. Controls were physically healthy and free of any history

Results

Neither the PEA threshold values, nor the UPSIT scores differed significantly between the depressed SAD patients and the control subjects, or within the patients across the light treatment conditions (Table 2). No significant difference was found between the mean R-UPSIT and L-UPSIT scores. However, in depressed patients, a negative relationship was present between R-UPSIT scores and the typical depression scores (r=−0.56, P=0.006); no correlation was present between L-UPSIT and typical

Discussion

The absence of a significant difference in olfactory performance between patients and controls is consistent with some previous studies in nonseasonal Amsterdam et al., 1987, Warner et al., 1990 and seasonal depression (Oren et al., 1995). These negative findings, however, are contradicted by other reports suggesting abnormal olfactory identification ability in patients with nonseasonal depression Serby et al., 1990, Rupp et al., 1997. Methodological differences, such as differences in

Acknowledgements

We are grateful to Dan Oren, MD for his encouragement and advise at the very beginning of the project. Ludy Yi and Mulon Luo contributed to bibliographic and data management. We thank Ronald Barnett, PhD; Frances Myers, RN, MSN, Holly Lowe, MSW, Todd Hardin, MS, Kathleen Dietrich, RN for screening and rating patients. Study supported by NIMH-intramural program and by NINCD grant PO1 00161, NIH.

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