Associations between olfactory identification and (social) cognitive functioning: A cross-sectional study in schizophrenia patients and healthy controls
Introduction
Schizophrenia patients have difficulties identifying odors (Moberg et al., 2014). The degree of this reduced odor identification (OI) compared to healthy controls has been examined extensively. A meta-analysis by Cohen et al. (2012) showed that OI in schizophrenia is nearly a standard deviation below the mean of controls.
Schizophrenia is also characterized by cognitive and social cognitive deficits, particularly in IQ, memory, processing speed, attention, executive functioning, emotion recognition and theory of mind (Mesholam-Gately et al., 2009). These deficits appear to be present before illness onset, as previous birth cohort studies showed that on average, subjects who later develop schizophrenia report poorer cognitive and social functioning in childhood and adolescence (Welham et al., 2009). Interestingly, impairments in social behavior and social cognition (i.e. emotion recognition) in schizophrenia have been related to OI deficit (Malaspina and Coleman, 2003, Kohler et al., 2007 resp.). Furthermore, previous studies have shown that OI and cognition are positively associated in schizophrenia (Brewer et al., 1996, Compton et al., 2006, Good et al., 2002, Goudsmit et al., 2004, Malaspina and Coleman, 2003, Moberg et al., 2006, Purdon, 1998, Saoud et al., 1998, Seckinger et al., 2004, Seidman et al., 1997, Seidman et al., 1991, Stedman and Clair, 1998) and in controls (Brewer et al., 1996, Compton et al., 2006, Seidman et al., 1991), with moderate strength in both groups. However, in the majority of these studies only one or two cognitive domains were examined in relation to OI and often a range of possible confounders such as age, gender, smoking and the use of antipsychotics associated with OI (Moberg et al., 2014) was not taken into account. Moreover, most studies lacked a control group.
Olfactory development is dependent on the development of frontal and temporal lobe areas (Nguyen et al., 2010, Turetsky et al., 2009) and its cognitive (i.e. IQ, memory, processing speed, attention, executive functioning) and social cognitive related functioning (Aleman, 2014). Since cognitive and social functioning in childhood and adolescence is already dependent on the brain maturation of these areas early in life we expect a relationship between OI and cognitive and social functioning in childhood and adolescence. To date, no studies have been performed linking OI to cognitive and social functioning in childhood and adolescence and to present state functioning on multiple social cognitive domains. In this study we therefore comprehensively examine whether OI is related to cognitive and social functioning in childhood and adolescent, as well as to a range of present state social cognitive domains in a large sample of schizophrenia patients and healthy controls. Furthermore, we aim to replicate whether olfactory functioning is associated with present state cognition.
Section snippets
Study design and population
Data from this cross-sectional study pertain to the multicenter ‘Genetic Risk and Outcome in Psychosis’- project (GROUP). This trial was part of an add-on study during the second measurement of this Dutch longitudinal GROUP–project. Participants were assessed extensively and were invited to participate in diagnostic interviews, questionnaires and neuropsychological tasks. The study protocol was approved by the accredited Medical Ethics Review Committee. All participants signed informed consent.
Sample characteristics
Table 1 summarizes socio-demographic differences between patients and controls. Clinical characteristics of patients are also summarized in Table 1. OI, cognitive and social functioning in childhood/adolescence, present state cognition and present state social cognition were significantly lower in patients compared to controls (see Table 2). Lower OI performance in patients compared to controls remained significant after correcting for gender, age, APD use and smoking. The R2 did not change
Discussion
In the largest group of schizophrenia patients (n = 132) and healthy controls (n = 128) up to date, we examined OI in relation to childhood and adolescent cognitive and social functioning as well as present state cognition and social cognition. The most original and novel finding of our study is that social and cognitive functioning in childhood/adolescence and present state social cognition domains of theory of mind and face recognition are related to OI.
We found that reduced OI was related to
Conflict of interest
Lieuwe de Haan has received research funding form Eli Lilly and honoraria for educational programs from Eli Lilly, Jansen Cilag, BMS, Astra Zeneca. Rene S. Kahn is or has been a member of DSMB for Janssen, Otsuka, Sunovion and Roche. Wiepke Cahn is or has been an unrestricted research grant holder with, or has received financial compensation as an independent symposium speaker or as a consultant from Eli Lilly, BMS, Lundbeck, Sanofi-Aventis, Janssen-Cilag, AstraZeneca and Schering-Plough. All
Funding
The infrastructure for the GROUP study is funded through the Geestkracht programme of the Dutch Health Research Council (ZON–MW, grant number 10–000–1001). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
Acknowledgment
We are grateful for the generosity of time and effort by the participants and their families, healthy subjects, and all researchers who make this GROUP–project possible.
References (35)
- et al.
Neuropsychological, olfactory, and hygiene deficits in men with negative symptom schizophrenia
Biol. Psych.
(1996) - et al.
Olfaction, “olfiction,” and the schizophrenia-spectrum: An updated meta-analysis on identification and acuity
Schizophr. Res.
(2012) - et al.
Associations between olfactory identification and verbal memory in patients with schizophrenia, first-degree relatives, and non-psychiatric controls
Schizophr. Res
(2006) - et al.
Unirhinal olfactory identification deficits in young male patients with schizophrenia and related disorders: association with impaired memory function
Schizophr. Res.
(2002) - et al.
Emotion processing in schizophrenia is state and trait dependent
Schizophr. Res.
(2015) - et al.
Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia
Schizophr. Res.
(2005) - et al.
Olfactory identification deficiency and WCST performance in men with schizophrenia
Psychiatry Res.
(1998) - et al.
Premorbid adjustment in schizophrenia−an important aspect of phenotype definition
Schizophr. Res.
(2007) - et al.
Olfactory identification and WAIS-R performance in deficit and nondeficit schizophrenia
Schizophr. Res.
(2004) - et al.
Neuropsychological probes of fronto-limbic system dysfunction in schizophrenia. Olfactory identification and Wisconsin Card Sorting performance
Schizophr. Res.
(1991)
Sex differences in olfactory identification and Wisconsin Card Sorting performance in schizophrenia: relationship to attention and verbal ability
Biol. Psychiatry
Neuropsychological, neurological and symptom correlates of impaired olfactory identification in schizophrenia
Schizophr. Res.
Olfactory functioning in schizophrenia and depression
Biol. Psychiatry
Neurocognitive basis of schizophrenia: information processing abnormalities and clues for treatment
Adv. Neurosci
Validity of the premorbid adjustment scale
Schizophr. Bull.
Measurement of premorbid adjustment in chronic schizophrenia
Schizophr. Bull.
Trail making and olfaction in schizophrenia: implications for processing speed
CNS Spectr.
Cited by (21)
Pleasant and unpleasant odor identification ability is associated with distinct dimensions of negative symptoms transdiagnostically in psychotic disorders
2022, Schizophrenia ResearchCitation Excerpt :Thus, our findings make the preliminary suggestion that pleasant and unpleasant olfactory impairments may have broad applicability as markers for avolition and inexpressivity across populations, and future work should attempt to replicate this in varied clinical and non-clinical samples. Our findings expand past suggestions of close associations between olfaction and social functioning in psychosis (Cumming et al., 2011; de Nijs et al., 2018; Malaspina and Coleman, 2003). Malaspina and Coleman (2003) postulated that olfactory deficits in schizophrenia are related to social dysfunction due to the link between olfaction and social affiliative drive in most mammals.
Olfactory modulation of the medial prefrontal cortex circuitry: Implications for social cognition
2022, Seminars in Cell and Developmental BiologyCitation Excerpt :As far as we are aware, three reports have been published on these interactions in patients with schizophrenia in a cross-sectional design. One study demonstrates a significant association of odor identification with theory of mind and face recognition in social cognition domains [145], and the other two studies report a significant relationship of odor identification with facial affect recognition [146,147]. In addition, similar findings are reported in other psychiatric conditions such as bipolar disorder and autism spectrum disorder [148–151].
Olfactory dysfunction and face processing of social cognition in first-episode psychosis
2022, Neuroscience ResearchCausal impact of local inflammation in the nasal cavity on higher brain function and cognition
2021, Neuroscience ResearchOlfactory dysfunction in frontotemporal dementia and psychiatric disorders: A systematic review
2020, Neuroscience and Biobehavioral Reviews