Impaired math achievement in patients with acute vestibular neuritis

Highlights

• Patients with acute vestibular neuritis show worse math performance.

• No difference in the number stroop task reflects intact number processing.

• Results are inconsistent with a number specific deficit (i.e., dyscalculia).

• Vestibular neuritis leads to a decline in executive functions.

Abstract

Broad cognitive difficulties have been reported in patients with peripheral vestibular deficit, especially in the domain of spatial cognition. Processing and manipulating numbers relies on the ability to use the inherent spatial features of numbers. It is thus conceivable that patients with acute peripheral vestibular deficit show impaired numerical cognition. Using the number Stroop task and a short math achievement test, we tested 20 patients with acute vestibular neuritis and 20 healthy, age-matched controls. On the one hand, patients showed normal congruency and distance effects in the number Stroop task, which is indicative of normal number magnitude processing. On the other hand, patients scored lower than healthy controls in the math achievement test. We provide evidence that the lower performance cannot be explained by either differences in prior math knowledge (i.e., education) or slower processing speed. Our results suggest that peripheral vestibular deficit negatively affects numerical cognition in terms of the efficient manipulation of numbers. We discuss the role of executive functions in math performance and argue that previously reported executive deficits in patients with peripheral vestibular deficit provide a plausible explanation for the lower math achievement scores. In light of the handicapping effects of impaired numerical cognition in daily living, it is crucial to further investigate the mechanisms that cause mathematical deficits in acute PVD and eventually develop adequate means for cognitive interventions.

Introduction

A peripheral vestibular deficit (PVD) leads to severe vertigo, nausea, vomiting, and imbalance (Brandt, 2003). Interestingly, in addition to the typical symptoms of PVD, patients frequently report having cognitive difficulties in daily life (Bigelow et al., 2015b, Black et al., 2004, Harun et al., 2015). These complaints have received empirical support in a growing body of evidence with regard to many cognitive domains including attention, memory, executive function, and spatial cognition (see Bigelow and Agrawal, 2015; Hanes and McCollum, 2006; Mast et al., 2014). It is intriguing that cognitive deficits have not only been found in dynamic situations (i.e., dual-tasks that combine cognitive tasks with postural challenges) but are also evident in static situations with no concomitant head or body movement (Redfern et al., 2004, Talkowski et al., 2005, Yardley et al., 2001).

Since the vestibular system is crucial for the cognitive representation of space (Angelaki and Cullen, 2008), deficits have been extensively studied in the area of visuo-spatial abilities (i.e., spatial cognition). It has been shown that bilateral vestibular failure is associated with hippocampal loss and impaired spatial navigation (Brandt et al., 2005, Kremmyda et al., 2016, Russell et al., 2003, Schautzer et al., 2003, Stackman and Herbert, 2002). Similarly, patients with unilateral PVD also perform worse than healthy controls in navigation tasks (Borel et al., 2004, Cohen, 2000, Guidetti et al., 2008, Péruch et al., 1999, Péruch et al., 2005 but see Hufner et al., 2007). Patients with PVD are also impaired in tasks that involve the mental rotation of one's own body without actual displacement (i.e, mental imagery; Candidi et al., 2013; Grabherr et al., 2011; Péruch et al., 2011; but see Deroualle et al., 2017). Taken together, there is strong evidence that PVD leads to an impaired internal representation of space (Borel et al., 2008).

The notion of impaired cognitive representation of space might not only explain the frequently found deficits in navigation and spatial memory following PVD. It may also play a crucial role in other cognitive functions that rely on rather abstract representations of magnitude and space. For example, the spatial organization of numbers has coined the term “mental number line” (Dehaene et al., 1993). These number-space associations are consistently found across various experimental paradigms. For example, in parity (odd vs. even) judgment tasks, participants typically respond faster to large numbers with the right hand, while responses to small numbers are faster with the left hand (SNARC effect; Nuerk et al., 2005). Other intriguing findings have been reported by means of random number generation tasks. Passive or active body-motion towards the left lead to the generation of smaller numbers compared to head motion towards the right (Hartmann et al., 2012, Loetscher et al., 2008, Shaki and Fischer, 2014).

Following this idea of number-space associations, Smith (2012) stated the hypothesis that there might be a link between PVD and dyscalculia. According to common definitions, individuals with dyscalculia perform poorly in mathematical achievement tests while showing normal intelligence (Butterworth, 2005; Butterworth et al., 2011; Cohen Kadosh and Walsh, 2007; von Aster and Shalev, 2007). At a lower cognitive level, the syndrome is characterized by a single core deficit in processing number magnitude (i.e., numerosity), which correlates with functional and anatomical abnormalities in parietal areas (Isaacs et al., 2001; Kucian et al., 2006; Mussolin et al., 2010; Price et al., 2007). Interestingly, there is first evidence in support of impaired processing and manipulation of numbers in vestibular disorders. Risey and Briner (1990) found that vestibular patients make more mistakes counting backwards, and score lower on the arithmetic subtests and the backward digit span task of the Wechsler Adult Intelligence Scale (WAIS). However, it has to be pointed out that the patients who took part in their study suffered from vertigo due to central origin. Nevertheless, deficits have also been found in patients with PVD in a double-task that required the participants to count backwards during a continuous body orientation task on an oscillatory chair (Yardley et al., 2002).

To date, despite ample anecdotal evidence of impaired numerical abilities in clinical practice, empirical evidence is still rather scarce. For example, it is yet unclear whether numerical deficits also appear under static conditions when no physical movements could interfere with cognitive processes. Furthermore, more research is needed to better specify which aspects of numerical cognition are impaired in patients with PVD. Poor mathematical skills can substantially impair performance at the workplace (Parsons and Bynner, 2005) and in daily life. Indeed, a recent report found that vestibular dysfunction was more strongly associated with difficulty managing finances than with motor-based activities of daily living (Harun et al., 2015).

In order to test the hypothesis of dyscalculia in patients with PVD, we set out to examine two key aspects that are implicated in dyscalculia. First, on a high level of numerical cognition, we wanted to investigate whether patients with PVD and healthy controls differ with respect to the efficient manipulation of numbers in complex tasks (i.e., math achievement). We expected that healthy controls outperform patients with PVD in a short math achievement test. Math achievement relies on a set of domain-general skills such as working memory or executive functions (De Rammelaere et al., 1999, DeStefano and LeFevre, 2004, Passolunghi and Pazzaglia, 2004, van der Sluis et al., 2007, von Aster and Shalev, 2007), which were repeatedly found to be impaired in vestibular dysfunction (Bigelow et al., 2015a, Black et al., 2004, Grimm et al., 1989, Hanes and McCollum, 2006, Moser et al., 2016).

Second, we were also interested whether PVD results in basic problems in processing the magnitude of numbers. Impaired performance in a number processing task would support the hypothesis of Smith (2012) since it is reflects a key aspect of dyscalculia. For this reason, we used the number Stroop task, which typically produces abnormal results in children and adults with impaired numerical cognition (e.g., Algom et al., 1996; Ashkenazi et al., 2009; Girelli et al., 2000; Rubinsten and Henik, 2005; Rubinsten et al., 2002). In its original form, the number Stroop task consists of two subtests, subsequently referred to as the physical and numerical number Stroop. Both subtests require the participants to compare two simultaneously presented digits. In the physical number Stroop, the participants are instructed to indicate which digit is physically larger (i.e., has the larger font size). In contrast, the numerical number Stroop requires a response to the digit that has the higher numerical value. The trials differ with respect to three congruity conditions. (1) Congruent trials consist of two digits, where one digit is larger with respect to both dimensions (i.e., physical size and numerical value). (2) In incongruent trials, the digit with the smaller numerical value is displayed with larger font size or vice versa. (3) In neutral trials, two identical digits are presented with different font size (physical subtest) or two different digits are presented with the same font size (numerical subtest).

First, we were motivated to investigate the size congruity effect (SCE), which refers to the difference in response times between congruent, incongruent, and neutral trials in the physical number Stroop. The SCE can be divided into a facilitation and interference component. Facilitation implies faster response times in congruent compared to neutral trials. Interference implies slower response times in incongruent compared to neutral trials. The SCE is considered to be a measure of automatic processing of the task-irrelevant number magnitude (Bugden and Ansari, 2011, Girelli et al., 2000, Rubinsten et al., 2002). Second, the number Stroop task allowed us to compare the distance effect, which is characterized by faster responses with increasing numerical distance between two simultaneously presented digits. For example, comparing two digits separated by a distance of 1 (e.g., “6” and “7”) leads to larger response time than comparing two digits separated by a distance of 5 (e.g., “2” and “7”). The distance effect serves as a marker of intentional number processing in the numerical number Stroop (Rubinsten et al., 2002). In contrast, a reversed distance effect (faster responses with decreasing numerical distance) has previously been observed in the physical number Stroop and has been interpreted as automatic number processing (Heine et al., 2010, Pina et al., 2015, Tang et al., 2006).

If patients with PVD suffer from a severe impairment of number magnitude processing similar to individuals with impaired numerical cognition (i.e., dyscalculia), we might observe a weaker SCE in the physical number Stroop (Ashkenazi et al., 2008, Ashkenazi et al., 2009, Girelli et al., 2000, Kadosh et al., 2007, Rubinsten and Henik, 2005, Rubinsten and Henik, 2009). Furthermore, we might expect a stronger distance effect in the numerical number Stroop, which is another typical finding in individuals with weak numerical cognition (Bugden and Ansari, 2011, De Smedt et al., 2009, Heine et al., 2010, Holloway and Ansari, 2009, Mussolin et al., 2010, Pina et al., 2015, Rubinsten et al., 2002, Tang et al., 2006). However, as mentioned above, the term “dyscalculia” usually refers to a learning disability, which is characterized by a specific deficiency in core numerical abilities with intact function in other cognitive domains (Butterworth, 2005, Butterworth et al., 2011, Cohen Kadosh and Walsh, 2007). Since cognitive deficits in PVD were frequently observed in non-numerical tasks (Bigelow and Agrawal, 2015, Hanes and McCollum, 2006, Mast et al., 2014, Smith et al., 2005), it is unclear whether numerical deficits in PVD follow a dyscalculic pattern of number Stroop performance (i.e., weaker SCE and/or stronger distance effect).