Selective effects of upper respiratory tract infection on cognition, mood and emotion processing: A prospective study
Introduction
Upper respiratory tract infections (URTIs), such as the common cold or influenza, are among the most common infections in human beings (Johnston and Holgate, 1996). The typical adult experiences between 2 and 5 infections per annum (Sperber, 1994). Such systemic infections, and their associated inflammatory response, may lead to behavioural changes, including changes in mood and cognition, commonly referred to as sickness behaviour (Hart, 1988, Dantzer et al., 1998). URTIs give rise to a spectrum of symptoms that include physical signs such as sneezing, sore throat, nasal congestion and sinus pain, and also have effects on the central nervous system, causing fever and malaise (Eccles, 2005). Many of these central effects are influenced by inflammatory mediators (Konsman et al., 2002), generated in the periphery, which in turn communicate with the brain. Even sub-pyrogenic levels of systemically administered endotoxin may give rise to changes in mood and cognition (Reichenberg et al., 2001). There is also evidence to suggest that systemic infections or inflammation may have profound effects on the aged or diseased brain (Perry et al., 2007). Thus, given the frequency of URTIs and the potential burden these infections may have on well-being and performance, it is important to understand more precisely the impact of these infections on brain function.
A number of studies has explored the effect of the common cold or influenza on cognition, either experimentally induced or naturally occurring. These suggest that responses to computerised reaction time (RT) measures, such as choice reaction time (CRT) and focussed attention, are slowed during experimentally induced infection (e.g. Smith et al., 1987a, Smith et al., 1987b, Smith et al., 1989, Smith et al., 1993, Smith, 1992; but see Drake et al., 2000) and during naturally occurring colds (Hall & Smith, 1996, Smith et al., 1998, Smith et al., 1999, Smith et al., 2004); although these studies found no correlation between the severity of reported symptoms and RTs. Some studies have reported negative impact on memory (Capuron et al., 1999, Smith et al., 1988), whilst others have not found this effect (Smith et al., 1993).
In a critical review, Savory (1992) argued that many studies suffered from methodological problems including a failure to report the severity of participants’ illness, poor matching of experimental and control participants, or a very limited range of cognitive tasks. Taken together, this suggests that the impact of URTIs needs to be investigated in a more methodologically rigorous manner, using better matching procedures, and a more comprehensive range of cognitive measures. To this end, we used a range of neuropsychological measures assessing working and secondary memory, plus memory speed (recognition and recall, in visual and verbal domains), as well as measures of attentional speed and accuracy (in simple and choice reaction, and vigilance tasks). Although previous studies have measured attention and/or memory this is the first to measure the speed of memory functioning as well as its accuracy. These tests result in robust factor scores, thus reducing the risk of a Type 1 error which would be present if each test were to be compared separately. In addition, given that negative effects on mood have been demonstrated using systemic endotoxin challenge (Reichenberg et al., 2001) and in URTIs (Smith et al., 2000) and that negative mood may be a feature of sickness behaviour in humans (Vollmer-Conna et al., 1997), these too must be assessed. Finally, we added assessments of emotion processing. Previous research has shown that URTIs impair attention and, variably, memory. Thus, we wished firstly to determine if the effect of URTIs on mood might extend to the perception of emotions in others. Secondly, tasks which require more complex attention and memory, having a greater evaluative component requiring recruitment of the frontal lobes, may be expected to be sensitive to URTIs, whereas those which rely on more automatic processes, thus needing fewer cognitive resources may be less affected by infection (Alexander et al., 1986, Mesulam, 1998; e.g. working memory involves the recruitment of the temporal lobes and the dorso-lateral and ventro-medial prefrontal cortices, Petrides, 2000). Two emotion processing tasks developed by Hariri et al. (2000) provided a contrast between more automatic (matching emotional faces to faces) and more complex (matching emotional faces to labels) processing requirements (Adolphs, 2002, Hariri et al., 2000) and these are used here.
This study was designed to investigate the impact of a naturally occurring URTI in healthy older and younger adults. A prospective, matched, case-controlled design was used to test effects on cognition, emotion processing and mood. We predicted that URTIs might significantly and negatively impact on higher order cognitive functions such as attention, working and secondary memory, and emotion processing (emotional face–label matching), but not on lower level emotional face–face matching. We also predicted that participants developing an URTI would have higher negative moods and lower positive moods at their second visit, than those well at both visits. Furthermore, given the particular vulnerability of older adults both to URTIs (Han and Meydani, 1999) and to changes in episodic memory, information processing speed and attention (Craik & Salthouse, 2000, Hedden & Gabrieli, 2002), we tested these effects separately in older and younger participants.
Section snippets
Participants
Eighty participants were recruited over two 10-week periods; 42 younger adults (Age M 20.3, SD 4.9, range: 18–43 years; five male, 37 female), 38 older adults (Age M 64.3, SD 39, range: 57–70 years; 15 male, 23 female). The first recruitment period ran from October to December 2005 (20 older and 22 younger adults), the second from January to March 2006 (18 older and 20 younger adults). Students were recruited through a research participation website, and received study credits. Older adults were
Participants
Following baseline assessment, 21 (26%) participants (11, 29% older adults, 10, 24% younger adults) contacted us regarding URTI symptoms. There was no age group difference in the distribution of participants becoming ill, X2 (1, N = 80) = 0.3, p = .602. Although the interval between baseline and falling ill was longer for older than younger adults, F(1, 38) = 5.0, p = .032, there was no main effect of Health Status and no Health Status by Age Group interaction, both F < 1, indicating that the interval
Discussion
This study examined the impact of a naturally occurring URTI on mood, emotion processing and cognition in older and younger healthy participants. We found that, despite having no fever, and in most cases no identifiable pathogen, self-reported illness significantly reduced participants’ speed of accessing stored memories, the speed of labelling facial emotions, and impaired their mood. Previous studies have reported a similar difficulty identifying infecting viruses in all participants, but
Acknowledgments
Romola Bucks is now at the School of Psychology, University of Western Australia. This study was funded by a Biotechnology and Biological Sciences Research Council Grant (BBS/B/15864). We are grateful to the members of the ‘Exploring the Mind’ volunteer panel, of the University of Southampton who participated in this study. With thanks to Alexandra Hogan and Anke Karl for their helpful comments on an early draft of this paper.
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