These findings suggest that the valence of the odor being identified differentially influences odor identification accuracy in schizophrenia patients, with no influence of sex, education, or race. Specifically, we observed that both males and females with schizophrenia displayed significantly reduced identification accuracy for normatively-defined pleasant and neutral odors while showing intact identification for unpleasant odors. These results coincide with a prior finding that patients with schizophrenia display aberrant hedonic ratings for pleasant but not unpleasant odors (Crespo-Facorro et al., 2001
). The results of the current investigation extend a prior investigation by Strauss et al. (2010)
in which the influence of valence on odor identification performance was examined in deficit and non-deficit patients with schizophrenia. These authors did not observe a differential pattern of identification accuracy for pleasant and unpleasant odors. Rather, patients had comparable levels of impairment for both pleasant and unpleasant odors. Consistent with the reported association between negative symptoms and olfactory impairments, deficit syndrome patients performed worse than non-deficit patients, but this was independent of odor valence. The discrepancy between our results and those of Strauss et al. (2010)
may reflect a number of methodological differences, including sample size, sample characteristics (predominantly male schizophrenia sample with longer illness duration), number of olfactory test items (40-item UPSIT vs. 12-item B-SIT), and the strategy for dealing with relatively neutral odors. Strauss et al. (2010)
classified all odors as either pleasant or unpleasant, which may have diluted the effects of strong negative hedonic valence. In particular, since odor identification performance deteriorates markedly with longer illness duration (Moberg et al., 1997
), the fact that their sample was ill for approximately 10 years more than our sample may have eliminated the valence effect that we observed.
Why might identification accuracy for unpleasant odors be preserved in patients, and why might this be associated, paradoxically, with greater levels of anhedonia and depression? We note that this finding is consistent with data indicating that schizophrenia patients have impaired visual recognition memory for positive valenced pictures, but preserved recognition memory for negative valenced pictures, especially those considered to be highly arousing (Herbener et al., 2007
). It has been proposed that individuals with schizophrenia have a bias for preferential processing of negative, potentially threat-related stimuli (Pause et al., 2008
) or, alternatively, that they fail to be motivated by potentially pleasant experiences (Herbener et al., 2007
). Imaging studies of olfaction suggest that individuals with schizophrenia rely more on prefrontal cortical regions and less on subcortical limbic structures to perform the task of evaluating negative odors (Crespo-Facorro et al., 2001
; Schneider et al., 2007
). This was interpreted as a compensatory response, in the context of an underlying limbic disturbance, when confronted with a potentially environmentally important negative or threatening stimulus. Greater reliance on prefrontal cortical processing may facilitate, almost as a byproduct, enhanced cognitive processing of these negative stimuli, resulting in improvement in the identification of negative valence odors. If this model is correct, then it would not be surprising that patients with greater levels of affective symptomatology – i.e., those with the greatest limbic dysfunction – would also be those with the greatest ability to identify negative odors.
The finding that hedonic odor identification is modulated by patients’ antipsychotic medication regimen may be either causative or merely coincidental. We observed a strong correlation between treatment with typical antipsychotic agents and levels of depression. It is possible that the side effects associated with these medications increased affective symptom ratings. Alternatively, this may be a serendipitous association in our sample. The current data set does not allow us to entirely differentiate these two possibilities. This would require patient subsamples with different treatment regimens but with comparable levels of affective symptomatology. It is notable, though, that our small subset of unmedicated patients exhibited the same performance profile as the entire patient sample. That is, they differed significantly from controls in their ability to identify pleasant and neutral odors, but not unpleasant odors. These results indicate that the findings from the current study cannot be attributed entirely to medication effects.
Consistent with previous work (Moberg et al., 1997
; Ugur et al., 2005
) overall odor identification accuracy was strongly associated with longer duration of illness. In addition, an association between duration of illness and identification accuracy for pleasant odors was observed, suggesting that degradation of olfactory abilities differentially affects pleasant odor identification over the course of the illness. Alternatively, it suggests that the processes underlying the preservation of unpleasant odor identification are resistant to the olfactory decline associated with greater chronicity.
Several limitations should be noted. First, our available data on smoking status did not include pack-years, which is considered a more reliable assessment of lifetime smoking behavior, but which may or may not accurately reflect the current impact of smoking. Though extant literature in both schizophrenia (for reviews, see: Martzke et al., 1997
; Moberg et al., 1999
) and healthy people (Frye et al., 1990
; Amoore, 1991
) has indicated a negligible impact of smoking on olfactory function, less is known about how smoking history influences odor valence perception. Second, subjective participant ratings of odor pleasantness were not ascertained. So, although patients’ identification performance varied with respect to normative differences in hedonic quality, we do not know how this relates to subjects’ own perceptions of hedonic valence. The current study was also limited by the specific odors used for assessment. Odors are typically described across a variety of dimensions including pleasantness, edibility, familiarity, and intensity. Although the UPSIT was constructed to balance these factors and, in particular, to select odors of comparable intensity (Doty et al., 1984
), subtle differences between odor groups on one or more of these dimensions may have influenced odor identification ability in our sample. Furthermore, there were a fewer number of unpleasant odorants assessed compared to pleasant and neutral odorants. Though standard deviations did not differ between the odor valence types, a balanced number of odorants for each valence would have been more helpful in comparing accuracy across subtypes. Lastly, our findings on relationships between mood states, medication status, and valence identification accuracy were preliminary given the methodological limitations of the current study. Future studies controlling for these limitations would be an important step in furthering our understanding of odor hedonic processing in schizophrenia and the influence of variables such as medication status and affective symptomatology.
Collectively, the results of the current study suggest that psychophysical probes of the olfactory network are relevant to difficulties with hedonic capacity observed in schizophrenia. While more research is needed to elucidate hedonic processing of odors in schizophrenia and its relationship both to structural and functional measures of brain function and to cognition, the findings of the current study suggest a preservation of processing for unpleasant odors. These findings highlight the need for additional research that examines the functional and structural deficits that underlie differences in odor valence identification in schizophrenia.