The relationship between autistic traits and olfactory performance in the general population

7.1 Introduction

The human olfactory system is remarkably sensitive to smells, with one study

demonstrating that a single molecule of odorant can excite a single olfactory receptor (which is the most sensitive the system can be) (De Vries & Stuiver, 1961). However, the number of receptors in the human olfactory system is much smaller than in other animals (resulting in a comparative loss of sensitivity), e.g. humans have 10 million receptors compared to dogs, who have 1 billion (Goldstein, 2002). Furthermore, smell can have a profound effect on many aspects of perception and cognition. For example, our perception of flavour is strongly affected by smell, and a loss of the former can have a profound impact on the ability to taste (Goldstein, 2002). In addition, there have been studies demonstrating that smells can have significant effects on emotion (Lehrner, Eckersberger, Walla, Pötsch, & Deecke, 2000), social preferences (Li, Moallem, Paller, & Gottfried, 2007), moral judgements (Schnall, Benton, & Harvey, 2008) and even behaviour regulation (Holland, Hendriks, & Aarts, 2005).

As previously discussed, it has been well established that individuals with ASD tend to report experiencing over-sensitivity and/or under-sensitivity to sensory stimuli in a variety of questionnaire-based studies (Baranek et al., 2006; Crane et al., 2009; Leekam et al., 2007; Talay-Ongan & Wood, 2000) Indeed, the planned draft for the next version of DSM-5 has included the presence of sensory issues in the criteria for ASD (American Psychiatric Association, 2010), an aspect that is absent from the most recent version of DSM (DSM-IV-TR: American Psychiatric Association, 2000). A large proportion of those with ASD tend to report atypical sensory sensitivity. For example, Leekam et al. (2007) reported that 94% of their autism sample experienced increased levels of sensory

atypicalities, compared with only 5% of typically developing children. However, it is also important to determine which mechanisms cause these different responses in ASD, so that greater insight into the causes and implications of ASD can be obtained.

Relatively few studies have experimentally investigated olfaction in ASD, with results being somewhat mixed. As was previously discussed in section 1.3.4, there is evidence that children with autism have raised detection thresholds for olfactory stimuli (Dudova et

al., 2011), although others have found no differences in thresholds for adults with ASD (Suzuki et al., 2003; Tavassoli & Baron-Cohen, 2012a). Furthermore, there are conflicting results in the identification abilities of those with ASD compared to TD comparison

groups, with some finding no significant group differences (Brewer et al., 2008; Dudova et al., 2011), others finding impaired performance in an identification task (Bennetto et al., 2007; Suzuki et al., 2003) and one study finding impaired performance for only those with a diagnosis of autism, rather than AS (May et al., 2011).

As mentioned in the Introduction (Chapter 1), there is evidence to suggest that those with higher levels of autistic traits (often referred to as exhibiting the ‘Broader Autism

Phenotype’) demonstrate similarities to those with an ASD. For example, it appears that brain structure and function are different in those with more autistic traits, with differences in the pSTS being identified (von dem Hagen et al., 2011). This brain region has been implicated in ASD, and is important in social and speech perception (Redcay, 2008). In addition, those with high levels of autistic traits have been shown to perform differently in both visual and auditory tasks compared to those with low levels of autistic traits, as discussed previously in Chapter 1. Furthermore, we recently found that self-reported sensory responsiveness to stimuli increased alongside an increase in autistic traits (see Chapter 2; Robertson & Simmons, 2012). However, as yet, there have been no studies reported which assess olfactory performance and the relationship with autistic traits.

It has been suggested recently that the atypical sensory responsiveness experienced by those with ASD could be a result of intra-participant variability caused by added noise in the neural system (Gowen & Hamilton, 2012; Milne, 2011; Simmons et al., 2009). The variability between those with ASD is often larger than observed in control groups (Milne, 2011), although few studies discuss the variance of responses observed in their samples. It may be that increased variance (both for responses given by each individual and for the group as a whole) could be indicative of increased noise in the perceptual system (see Simmons et al., 2009, for more detail).

In this study, we assessed various aspects of olfactory performance in the general

population (threshold, discrimination and identification) and analysed the relationship with autistic traits. Furthermore, we administered the sensory questionnaire described in

Chapter 2 to a sub-group of the sample, in order to a) determine whether the same, positive relationship between scores on the GSQ and AQ was observed and b) to observe whether perceived over- or under-sensitivity to olfactory stimuli was related to absolute thresholds.

Furthermore, we were interested in analysing intra-participant variability for the threshold test. Our main hypotheses were as follows:

• There would be no significant differences between high and low AQ scorers for the threshold, discrimination and identification tasks

• Those with high AQ scores would demonstrate higher intra-participant variability for thresholds compared to low AQ scores

• A positive, significant correlation between GSQ and AQ scores would be observed in the sample

7.2 Methods

7.2.1 – Participants

106 people (74 females; 32 males) participated in this experiment (mean age = 24 years 4.42 months ± 6 years 1.96 months). Those with the highest 15% (n = 17; mean score = 27.82 ± 5.64) and lowest 15% (n = 18; mean score = 6.33 ± 1.57) of scores in the AQ formed the ‘high’ and ‘low’ scorers groups (Low: AQ from 4 – 8; High: AQ from 22 – 45) and were compared in various aspects of their olfactory functioning.

A number (n=41) of participants were recruited by an undergraduate student (as part of her final year project), with the author obtaining the remaining participants (n=65). Both stages of data collection were carried out in the same way, apart from the inclusion of the GSQ in the author’s collection of data (i.e. the GSQ was not included in the undergraduate student’s study). Due to time constraints, some participants were not able to complete the GSQ during the session (n=3). Therefore, 62 of 106 participants completed the GSQ, with all 106 participants completing the olfactory experiments and the AQ. Participants were recruited using the University of Glasgow subject pool, which mainly consists of

undergraduate and postgraduate students. Each session took approximately 1 hour, and participants were either paid £6 for their time (n=63) or given undergraduate course credits (n=43).

7.2.2 – Apparatus

The Sniffin’ Sticks Extended Test (Burghart, Messtechnik) was used to measure the olfactory functioning of participants. This is a standardized, commercially available test that assesses three aspects of olfactory functioning (threshold, discrimination and

identification) (Hummel, Sekinger, Wolf, Pauli, & Kobal, 1997).

Olfactory thresholds were established using the ‘Threshold’ section of the Sniffin’ Sticks Extended Test. This test consists of 16 pens filled with varying concentrations of n-butanol diluted in propylene glycol (with pen 1 being the strongest and pen 16 being the weakest). Three pens are sequentially presented to the participant, with only one having an odour. The participant is asked to discriminate the pen that has an odour from the

odourless pens. In the odour discrimination task, the experimenter presents triplets of pens (two with the same odour and a third with a different odour) to the participant. The

participant is asked to determine which smell is different. Identification performance is assessed by the administration of sixteen common odours. The participant is asked to identify the odour from a list of four presented alongside each pen.

7.2.2.2 – Questionnaires Autism Spectrum Quotient (AQ)

See section 2.2.2 for details of the AQ.

Glasgow Sensory Questionnaire (GSQ) See section 2.2.2 for details of the GSQ.

7.2.3 – Procedure

Participants were asked to ensure that they did not eat or drink anything (apart from water) for 15 mins prior to the start of the experiment. As suggested in the Sniffin’ Sticks

manual, the tests were presented in the following order: Threshold – Discrimination – Identification. In addition, participants were not given feedback on their performance during any of the olfactory tasks. Questionnaires were presented in between olfactory tasks, with their order counter-balanced across the sample. The procedural details for the olfactory tasks were as follows.

Thresholds

Participants were blindfolded during the threshold task, in order to prevent visual

information affecting performance. Odour thresholds were determined using an ascending staircase, triple-forced choice paradigm. Participants were presented with triplets of pens, with each pen presented for around 3 seconds and leaving a 5 second interval before the next pen was presented. As detailed in the manual, there was a minimum of 30 secs between the first pen of one triplet and the first pen of the next triplet being presented.

Pens were presented in the following repeating order across trials: TARGET – BLANK – BLANK; BLANK – TARGET – BLANK; BLANK – BLANK – TARGET. The task starts with either dilution level 16 or 15 (16: n=53; 15: n=53) and the concentration ascends in 2-dilution steps (e.g. 16-14-12 or 15-13-11) until the participant identifies the target pen in two sequential trials. The staircase then reverses and continues until the participant gives an incorrect answer. Seven reversals are determined for each participant, with the

threshold being computed from the mean of the final four reversals. A visual illustration of this process is presented in Table 7.1 (Ticks are correct answers and crosses are incorrect answers).

Table 7.1 – Demonstration of identifying thresholds

10 ✔✔

11 ✔✔ ✔✔ ✔✔ ✔✔

12 ✔ X ✔ X ✔✔ X X

13 ✔ X

14 X

15

16 X

Illustration of how thresholds are established using the Sniffin’ Sticks task. The ‘turning points’

are coloured red: 13, 11, 12 and 11, which would indicate a threshold of 11.75.

Possible scores on this task range from 0 (unable to detect any of the concentrations) to 16 (consistently able to detect the lowest concentration). As well as determining each

person’s threshold, we analysed the distance of the threshold from each turning point (as we were interested in whether this varied between participants) in order to assess intra-participant variability. This process can be illustrated using the data in Figure 7.1. The mean threshold is 11.75, and the distance of each turning point from the mean is computed (i.e. 1.25, 0.75, 0.25 and 0.75 respectively), with an overall mean of this distance computed from these values (which, in this example, is 0.75).

Discrimination

Participants were blindfolded during the discrimination task, in order to prevent visual information affecting performance. Discrimination ability was determined using a triple-forced choice paradigm. Participants were presented with triplets of pens, with each pen presented for around 3 seconds and leaving a 5 second interval before the next pen was presented. As detailed in the manual, there was a minimum of 30 secs between the first

pen of one triplet and the first pen of the next triplet being presented. Pens were presented in the following repeating order across trials: SAME – DIFF – SAME; SAME – SAME – DIFF; DIFF – SAME – SAME. Participants were required to determine which of the odours smelled different from the other two. Possible scores ranged from 0 (incorrect discrimination on all trials) to 16 (correct discrimination on all trials).

Identification

Participants were not blindfolded during the identification task. In order to assess their olfactory identification ability, they were asked to choose which odour they had been presented with from a choice of four. There were 16 odours in total and resulting scores ranged from 0 (incorrect identification on all trials) to 16 (correct identification on all trials).

7.3 Results