Introduction: Patients with vestibular disorders sometimes report cognitive difficulties, but there is no consensus about the type or degree of cognitive complaint. We therefore investigated subjective cognitive dysfunction in a well-defined sample of neuro-otology patients and used demographic factors and scores from a measure of depression, anxiety, and stress to control for potential confounding factors. Methods: We asked 126 neuro-otology clinic outpatients whether they experienced difficulties with thinking, memory, or concentration as a result of dizziness or vertigo. They and 42 nonvertiginous control subjects also completed the Neuropsychological Vertigo Inventory (NVI, which measures cognitive, emotional, vision, and motor complaints), the Everyday Memory Questionnaire (EMQ), and Depression, Anxiety, and Stress Scales (DASS). Results: In the initial interview questions, 60% of patients reported experiencing cognitive difficulties. Cognitive questionnaire scores were positively correlated with the overall DASS score and to a lesser extent with age and gender. Therefore, we compared patients and controls on the NVI and EMQ, using these mood and demographic variables as covariates. Linear regression analyses revealed that patients scored significantly worse on the total NVI, NVI cognitive composite, and 3 individual NVI cognition subscales (Attention, Space Perception, and Time Perception), but not the EMQ. Patients also scored significantly worse on the NVI Emotion and Motor subscales. Conclusions: Patients with dizziness and vertigo reported high levels of cognitive dysfunction, affecting attention, perceptions of space and time. Although perceptions of cognitive dysfunction were correlated with emotional distress, they were significantly elevated in patients over and above the impact of depression, anxiety, or stress.

There is a growing body of literature on the role of the vestibular system in cognition. Behavioral studies in animals and humans with vestibular lesions have shown deficits in navigation and spatial memory [Smith and Zheng, 2013; Mast et al., 2014]. These are accompanied by anatomical and physiological changes to areas of the brain that receive vestibular input, including the temporoparietal junction, parietal cortex, cingulate gyrus, retrosplenial cortex, and the hippocampal and parahippocampal cortices [Shinder and Taube, 2010; Hitier et al., 2014]. The distributed nature of vestibular information throughout the brain suggests that a loss or disturbance of vestibular information has the potential to interfere with a variety of cognitive functions. Patients attending neuro-otology clinics often report cognitive difficulties or “brain fog” [Black et al., 2004; Agrawal et al., 2013], yet there remains little information about the nature and extent of cognitive complaints in patients with vestibular disease. As vertigo and dizziness are significantly associated with depression and anxiety, which also have effects on cognition [Millan et al., 2012], distinguishing the effects of vestibular disease and psychological distress on cognition is difficult.

Several studies of subjective cognitive dysfunction in patients with vertigo have been published in recent years. A large survey of the adult population in the United States found that of the 8% of respondents reporting vestibular vertigo, 12% reported activity limitation because of memory difficulties or confusion, and about a third of this relationship was mediated by depression, anxiety, or panic disorder [Bigelow et al., 2016]. Bisdorff et al. [2015] investigated memory complaints on the Questionnaire for the Self-Evaluation of Memory (QAM) in a well-defined sample of 50 patients with common vestibular diagnoses. They found that patients reported greater memory difficulties than controls, but the degree of impairment was better predicted by comorbid psychological distress than the severity of vertigo. Lacroix et al. [2016] developed a French language questionnaire specifically for patients with vertigo, the Neuropsychological Vertigo Inventory (NVI) [Lacroix et al., 2016]. The questionnaire had 4 subscales addressing aspects of cognition (Attention, Space Perception, Time Perception, and Memory) and 3 subscales on Emotion, Vision, and Motor function. Patients (N = 108) had higher scores (more dysfunction) on the NVI total score and higher scores on the Attention, Emotion, Vision, and Motor subscales than controls (N = 104) but not on the other cognitive subscales. The absence of effect on 3 of the 4 cognitive subscales may have been due to sample characteristics, as patients were recruited from patient associations rather than medical clinics, and emotional distress was not measured. Liu et al. [2019] more recently used an English language version of the NVI in a group of 67 formally diagnosed neuro-otology patients. They found higher levels of subjective cognitive dysfunction in patients with Meniere’s disease (MD) and vestibular migraine (VM) than benign paroxysmal positioning vertigo (BPPV) and reported that depression and anxiety mediated this effect, but the patients were not compared to a control group. Finally, Rizk et al. [2020] reported elevated scores on the Cognitive Failures Questionnaire in patients with vestibular disease. They found that patients with persistent postural-perceptual dizziness (PPPD) reported the most cognitive problems, followed by patients with VM plus MD, while those with BPPV reported the least problems. Patients with PPPD and VM plus MD had elevated scores compared to published normative data, while those with other diagnoses had similar or lower scores, but patients were not compared to a control group and there was no assessment of psychological distress.

These studies provide important data about the cognitive complaints of neuro-otology patients, but there is no consensus about the range or degree of these complaints and inconsistency in the use of control groups and measures of psychological distress. The aim of the current study was to investigate subjective cognitive dysfunction in a representative sample of patients with vertigo, dizziness, or imbalance attending a specialist neuro-otology outpatient clinic. We compared patient scores to those of a control sample and used demographic factors and a measure of depression, anxiety, and stress to control for the potential confounding effects of psychological distress.

Participants

We recruited adult neuro-otology patients and controls during a 7-week period of data collection between December 2017 and February 2018 from the waiting rooms of a specialist neuro-otologist (author M.S.W.). The patients attended either an outpatient clinic for neuro-otology or a specialized clinic for BPPV at Royal Prince Alfred Hospital (RPAH), Sydney. One investigator (author D.X.) approached all patients who attended the clinics for dizziness, vertigo, or imbalance and excluded patients who had insufficient English language ability or neurological conditions that could affect cognition (such as dementia, stroke, and head injury). The controls consisted of friends or relatives who accompanied the patient to the appointment. They did not suffer from dizziness or vertigo and were subjected to the same exclusion criteria. We assumed that the controls would provide a degree of matching in terms of socioeconomic status and education level. All participants gave written informed consent according to the Declaration of Helsinki. The study was approved by the Local Ethics Committee (X13-0425 & X18-0097, HREC/18/RPAH/136).

Of 172 patients approached and asked to participate in this study, 166 were willing to participate. Of these, 18 were excluded (at the time or after chart review) due to the presence of a neurological condition that might have produced cognitive symptoms. Another 5 patients were excluded as they did not attend the clinic for dizziness, vertigo, or imbalance, and for 2 patients, there was insufficient clinical information available for classification. A further 15 patients who originally expressed willingness were unable to participate in the study due to time constraints (N = 9), insufficient English language ability (N = 3), or feeling too unwell on the day (N = 3). There were 126 patients in the final sample. Forty-three accompanying persons participated as control subjects, though one was excluded due to the presence of a neurological condition. The demographic details of the sample are given in Table 1. Patients were significantly older than controls (mean age difference 8.9 years, 95% CI 3.9–13.8, p < 0.001), and there were slightly more females than males in both groups, though there was no significant difference between the 2 groups in terms of gender distribution (χ2(1) = 0.13, p = 0.719). More than half of the patients (71, 56%) attended the clinic for a follow-up appointment, while 44% were new patients. Most patients (106, 84%) were recruited from the general neuro-otology clinic, while the remainder were recruited from the specialized clinic for diagnosis of BPPV.

Table 1.

Demographic details and scores on the DASS and DHI in patients and controls

 Demographic details and scores on the DASS and DHI in patients and controls
 Demographic details and scores on the DASS and DHI in patients and controls

A chart review was conducted in the months following data collection to determine patient diagnoses. Diagnoses were based on the current diagnostic criteria for the major vestibular diseases. Patients with VM were classified as definite or probable, depending on the clinical information available [Lempert et al., 2012]. Patients who did not meet these criteria, but who were treated clinically as “possible” VM patients, were included in this category. Those with MD were included if they had definite or probable MD according to Lopez-Escamez et al. [2015]. BPPV was diagnosed based on the results of Dix-Hallpike testing according to von Brevern et al. [2015]. Other, less-common diagnoses were based on symptoms, clinical signs, test results, and formal diagnostic criteria, as appropriate. Patients whose diagnosis could not be established were classified “unclear.” The most common diagnosis was probable or definite VM, either alone or in combination with another diagnosis. There were 87 patients with a single diagnosis, of which 45 had VM, 15 had BPPV, 13 had MD, 8 had vestibular neuritis or unilateral vestibular loss due to another cause, and 4 had bilateral vestibular loss. There was one patient each with vestibular paroxysmia, vestibular schwannoma, cerebellar disease, mal de debarquement, and PPPD. The remaining patients had either a combination of diagnoses (N = 19, e.g., BPPV secondary to vestibular neuritis) or the diagnosis was unclear at the time of publication, but the differential diagnosis involved common vestibular conditions (N = 17, e.g., VM vs. MD). There were 85 patients with episodic vertigo (i.e., VM, BPPV, MD, or a combination of these) and 49 patients with vestibular disorders that could be localized to the periphery, that is, the end organ or vestibular nerve (e.g., vestibular neuritis, BPPV, MD, vestibular schwannoma, some cases of bilateral vestibulopathy, or combinations of these).

Questionnaires

Neuropsychological Vertigo Inventory

An English language version of the NVI was provided by its authors [Lacroix et al., 2016]. This version was translated by Dr. R. Srinivasa Raghavan’s team using a double translation method. It consisted of 28 main items, divided into 7 subscales with 4 items each, and an additional distractor subscale with 4 items. There were 4 subscales about cognitive issues: Attention (including questions about difficulty concentrating, absent-mindedness, distractibility, and difficulty organizing oneself), Space Perception (about navigation and wayfinding, i.e., having a poor sense of direction, difficulty locating oneself on a map, setting off in the wrong direction, and having difficulty finding the way back), Time Perception (about orientation to time, i.e., difficulty recalling the current day of the week, the year, and the season, as well as difficulty placing historical events in the right chronological order), and Memory (with questions about having memory problems in general, difficulty remembering names, and forgetting appointments, birthdays, or anniversaries). The other 3 subscales were about Emotion, Vision, and Motor problems. Items were rated on a 5-point Likert scale (where 1 = never or strongly disagree and 5 = all the time or strongly agree). The maximum score without distractor items was 140 points (“NVI total”). We also calculated the total of the 4 cognitive subscales to obtain a combined cognitive score without the influence of emotion or physical symptoms (“NVI cognitive”). We used a pencil-and-paper version of the test in which the subscale and item order were fixed, in the order reported above, and with the distractor items interspersed. Distractor items were not analyzed further.

Everyday Memory Questionnaire

We used the 28-item version of the Everyday Memory Questionnaire (EMQ) as an additional means of investigating subjective memory complaints [Sunderland et al. 1984; Richardson and Chan, 1995; Cornish, 2000]. Each question is answered on a 9-point scale, in which 1 = not at all and 8 = more than once a day, and the total possible score is 228. Two-factor analyses of EMQ scores have suggested that the EMQ assesses various aspects of memory, including memory for recent events and activities, memory for words and faces, ability to monitor tasks and conversations, and spatial memory [Richardson and Chan, 1995; Cornish, 2000]. Questions that loaded onto the spatial memory factor in each study were summed to form 2 additional spatial memory measures to compare with the Space Perception subscale of the NVI. The “spatial memory” factor described by Cornish [2000], who tested 277 undergraduate students and found a 5-factor solution, included 4 questions: “Getting lost or turning in the wrong direction on a journey, on a walk or in a building where you have often been before,” “Getting lost or turning in the wrong direction on a journey, on a walk or in a building where you have only been once or twice before,” “Forgetting where things are normally kept or looking for them in the wrong place,” and “Forgetting details of things you do regularly, whether at home or at work. For example, forgetting details of what to do, or forgetting at what time to do it.” Richardson and Chan [1995] used the original 35-item version of the questionnaire in a sample of 115 patients with multiple sclerosis and 115 of the patients’ relatives. They also found a 5-factor solution, and their “route-finding” factor had 5 questions, including the first 2 questions listed above and 3 additional questions: “Failing to recognize places that you are told you have been to before,” “Not remembering changes in you daily routine, such as a change in the place where something is kept or a change in the time something happens,” and “Finding a television story difficult to follow.” The total possible scores for the “spatial memory” factor and for the “route-finding” factor were 32 and 40, respectively.

The Depression, Anxiety, and Stress Scales (DASS) is a self-report measure of depression, anxiety, and stress symptoms. The DASS consists of 42 items rated on a 4-point severity/frequency scale, where 0 = did not apply to me at all and 3 = applied to me very much, or most of the time [Lovibond and Lovibond, 1995]. The total score was used in all analyses, with the maximum score being 126.

Dizziness Handicap Inventory

The Dizziness Handicap Inventory (DHI) is a questionnaire about the impact of dizziness on daily activities and consists of 25 items on aspects of physical (6 items), emotional (9 items), and functional (10 items) impairment [Jacobson and Newman, 1990]. The maximum possible score is 100, and patients rate symptoms on a 3-point scale, where 0 = no, 2 = sometimes, and 4 = always. A total score of 0–30 indicates mild symptoms, 31–60 moderate symptoms, and 61–100 severe symptoms [Whitney et al., 2004].

Procedure

Participants were recruited from the waiting room before their appointment. Patients were first asked, “Do you have any difficulties with thinking, memory or concentration as a result of your dizziness, vertigo, or imbalance?” Those who reported difficulties were asked to describe them. Participants were then asked to complete the 4 written questionnaires in the following order: NVI, DASS, EMQ, and DHI. All 126 patients completed the NVI, 116 patients completed the DASS, 114 completed the EMQ, and 115 completed the DHI. All control subjects completed all 4 questionnaires, except for 1 subject who failed to complete the DASS and EMQ. The data collection took approximately 30 min and was completed on the same day. Patients sometimes required additional time after their appointment to complete the questionnaires.

Data Analysis

Pearson χ2 was used to compare proportions of males and females between groups. Relationships between selected continuous variables were compared using Pearson’s correlations. A linear regression analysis within the framework of generalized estimating equations (GEEs) was performed to determine the difference between patients and controls on the outcome measures. We first compared the ages of the patient and control groups. In all subsequent analyses, age and gender were added to the model to adjust for possible confounding effects, as these demographic factors may have effects on subjective cognitive impairment [Derouesne et al. 1993; Kim et al., 2003]. For this purpose, age was converted to a categorical variable. Age groups were <40, 40–55, 56–70, and >70 years of age. The principal GEE outcome measures were DASS and DHI total scores, NVI total and NVI cognitive scores, individual NVI subscale scores, and the EMQ overall score. For all analyses of NVI and EMQ scores, DASS scores were included in the model to adjust for possible confounding effects. For this purpose, DASS scores for the individual depression, anxiety, and stress scales were first converted to z-scores and then averaged to form a total score, using normal data and procedures described in the DASS manual [Lovibond and Lovibond, 1995]. Three DASS categories were formed using z scores −2 to 0.99, 1–1.99, and ≥2. Additional GEE analyses on subsets of data were performed to explore effects on collections of items from the EMQ and in patients with particular diagnoses. Results with p < 0.05 were considered statistically significant, and outcomes are reported as “mean difference between groups, 95% CI, p value.” Due to the exploratory nature of this study, there was no correction for multiple comparisons. Statistical analyses were performed with SPSS (version 25).

Initial Questions about Cognitive Difficulties

On questioning, 75 patients (60%) said they had noticed problems with thinking, memory, or concentration due to their dizziness, vertigo, or imbalance. On open-ended questioning, they described symptoms such as “fuzziness in the head,” “slower processing,” feeling “spaced out,” or having a “scrambled” memory. Many patients mentioned difficulty concentrating. For example, 1 patient said his concentration faltered during a vertigo attack as he was focused on stability and not falling. Some patients said they had previously experienced symptoms, but now that their dizziness had abated, and their concentration and memory had improved. On the other hand, some patients who did not report cognitive difficulties explained that it was hard to attribute symptoms to vestibular disease as opposed to other factors, such as aging.

Demographic Factors

Age had a significant effect on the NVI total score; the NVI Attention, Emotion, and Vision subscales; and the EMQ (after adjusting for group, gender, and DASS, χ2(1) = 2.5–19.7, ps ≤ 0.003). Older participants reported lower levels of dysfunction than younger participants. Gender had a significant effect on only the NVI Space Perception subscale, whereby females reported greater dysfunction than males (after adjusting for group, age, and DASS, χ2(1) = 1.8, p < 0.001).

Measures of Psychological Distress and Functional Disability

On the DASS, most patients and controls reported overall levels of depression, anxiety, and stress in the normal to mild range (z-score −1 to 0.99, patients 64%, controls 98%). Some participants, however, reported levels in the moderate range (z-score 1–1.99, patients 25%, controls 0%) or the severe to extremely severe range (z-score ≥2, patients 11%, controls 2%). On the DHI, 38% of patients reported dizziness handicap in the mild range, 46% in the moderate range, and 15% in the severe range. All of the controls reported scores in the mild range, with 75% having a score of 0 and the highest score being 16.

Overall, patients reported significantly more depression, anxiety, and stress than controls (mean DASS score difference 18.3, CI 12.4–24.3, p < 0.001) and had much higher scores on the DHI (33.1, 28.5–37.7, p < 0.001) (Table 1). Both measures were significantly correlated with total scores on the NVI and EMQ (DASS and NVI r = 0.65, DASS and EMQ r = 0.49; DHI and NVI r = 0.59, DHI and EMQ r = 0.34; all ps < 0.001). DASS scores had a significant effect on all NVI and EMQ outcome measures (i.e., after adjusting for group, age, and gender, Wald χ2(1) = 2.7–42.6, p ≤ 0.008). Participants with greater levels of depression, anxiety, and stress reported higher levels of cognitive dysfunction.

Measures of Cognitive Issues

Patients reported significantly higher levels of difficulty than controls on the NVI total; the cognitive score; and the Space, Time, Attention, Emotion, and Motor subscales, after adjusting for the potentially confounding effects of age, gender, and DASS score. There was a trend toward a significant difference between groups on the Vision subscale of the NVI and the EMQ; however, there was no difference on the Memory subscale of the NVI. Raw questionnaire scores and mean adjusted differences between groups, CIs, and p values are shown in Table 2. In the patients, scores on the EMQ were significantly correlated with the NVI Memory subscale score (r = 0.68), NVI cognitive score (r = 0.66), and NVI total score (r = 0.68, all p < 0.001).

Table 2.

Raw questionnaire scores and differences in adjusted means between patients and controls on the NVI and its subscales and the EMQ

 Raw questionnaire scores and differences in adjusted means between patients and controls on the NVI and its subscales and the EMQ
 Raw questionnaire scores and differences in adjusted means between patients and controls on the NVI and its subscales and the EMQ

Patients did not report significantly more difficulty than controls on the subset of EMQ questions related to “route-finding,” as described by Richardson and Chan [1995], after controlling for age, gender, and DASS score (mean difference 1.3, CI −0.1 to 2.8, p = 0.082). There was also no significant difference between the groups on the “spatial memory” questions reported by Cornish [2000] (mean difference 0.6, CI −0.8 to 2.0, p = 0.378). In the patients, both subsets of EMQ questions were significantly correlated with the Space Perception subscale of the NVI (“route-finding” vs. Space Perception r = 0.50, p < 0.001, “spatial memory” vs. Space Perception r = 0.48, p < 0.001).

Consideration of Different Patient Groups

Three additional analyses were performed to examine subjective cognitive difficulty in patients with particular diagnoses, again controlling for the effects of age, gender, and DASS score, and the results are shown in Table 3. We first compared patients with a sole diagnosis of VM to controls and found that patients scored worse on the NVI Attention subscale, as well as the NVI cognitive and total scores, but not on the Space Perception, Time Perception, or Memory subscales or the EMQ. VM was the only diagnosis with sufficient numbers of patients for such analysis. We then compared all patients with a peripheral cause of their vestibular disorder with controls. This included patients with multiple causes of vertigo, where both causes could be localized to the periphery, such as BPPV and vestibular neuritis. In this group, patients reported significantly more difficulties than controls on the Space Perception, Time Perception, and Attention subscales. Finally, we compared all patients with episodic vertigo, rather than chronic vestibular loss, to controls and found that patients scored significantly higher on the Space Perception and Attention subscales, while there was a trend toward a significant difference on the Time Perception scale.

Table 3.

Additional comparisons between groups of patients and controls

 Additional comparisons between groups of patients and controls
 Additional comparisons between groups of patients and controls

On direct questioning, more than half (60%) of our neuro-otology patients reported experiencing cognitive dysfunction as a result of their condition. On the questionnaires, the patients reported significantly more cognitive issues than controls; higher levels of depression, anxiety, and stress; and greater functional disability. More specifically, on the NVI, patients reported significantly greater difficulties in attention and perceptions of space and time than controls, as well as more motor problems on the noncognitive subscales. There was no significant difference between groups on either of the memory scales. The findings were similar, though generally weaker, when patients were grouped according to the type or distribution of disease.

The strengths of the current study include the relatively large sample of patients with confirmed diagnoses, use of a control group, and inclusion of a measure of psychological distress. The latter 2 are important as many of the symptoms we sampled have high base rates in the general population [Kroenke and Price, 1993; Wong et al., 1994; Chan, 2001; Wiltink et al., 2009; Garden and Sullivan, 2010; Bigelow et al., 2016; Neuhauser, 2016]. Importantly, psychological distress is associated with both dizziness and cognitive dysfunction [Haug et al., 2004; Lenze et al., 2005; Garden and Sullivan, 2010; Millan et al., 2012] and may mediate any effect of dizziness on cognitive complaints [Bisdorff et al. 2015; Liu et al., 2019]. Our results confirmed previous reports of greater psychological distress in patients with vertigo and dizziness compared to controls [Sloane et al., 1994; Grunfeld et al., 2003; Eckhardt-Henn et al., 2008; Roh et al., 2017]. While most patients reported only mild levels of depression and/or anxiety, 36% reported moderate or severe symptoms, considerably more than the control group (2%). As expected, patients and controls with greater levels of psychological distress reported more cognitive difficulties and greater functional impairment as measured by the DHI. However, when we accounted for these associations statistically, the patients in our study still reported more subjective cognitive dysfunction than controls.

Our findings are similar to previous studies of the NVI in neuro-otology patients. Total unadjusted scores on the NVI in our patient sample (69.7) were comparable with those reported by Lacroix et al. [2016] (67.6) and Liu et al. [2019] (VM 67.5, MD 67.3, BPPV 51.0), and scores for control participants (57.7) are also similar to those reported by Lacroix et al. [2016] (58.7). In terms of the cognitive domains assessed by the NVI, the largest and most consistent effect was seen on the Attention subscale, followed by the Space and Time Perception subscales, with no effect seen on the Memory subscale. In the original publication of the NVI, Lacroix et al. [2016] found higher scores for the Attention subscale in their patients, but no difference for the other 3 cognitive subscales. It is possible that our positive findings for the Space and Time Perception subscales are related to differences in our sample and/or study design, as we tested patients attending a neuro-otology outpatient clinic who had been diagnosed with vestibular disease and factored psychological distress and demographic factors into our analyses. Like Lacroix et al. [2016], we found that older patients reported fewer cognitive complaints on the NVI, and a similar effect was seen for the EMQ. Studies on the effects of age on subjective cognitive dysfunction have shown mixed results [Sunderland et al., 1986], and as hypothesized by Lacroix et al. [2016], the effect may be due to working-age patients experiencing greater cognitive demands and therefore having greater susceptibility to the perceived cognitive effects of vertigo.

On the Attention subscale, patients had consistently higher scores than controls, and the mean adjusted difference between patient and control scores was 1.8–2.1 points (out of a possible 20). Problems with concentration were commonly mentioned by patients when asked to describe their symptoms in detail. While these symptoms may be an indirect consequence of having an illness or feeling unwell, a likely contributor to this effect is that a disruption of the balance system causes patients to direct some of their attention to posture and gait, leaving fewer attentional resources available for other processes. There is evidence from dual-task studies that performance on mental tasks during concurrent balance tasks is diminished in patients with vestibular disease compared to that in controls [Yardley et al., 2001; Yardley et al., 2002; Redfern et al., 2004]. Balance and posture are usually less affected than the cognitive task, indicating a prioritization of postural control [Yardley et al., 2001; Redfern et al., 2004]. The reduced performance on cognitive tasks appears to occur regardless of how well a patient has compensated for the vestibular loss [Redfern et al., 2004] and can also be seen in normal volunteers tested during a challenging postural task [Yardley et al., 2001]. This aligns with some patients’ reports that they noticed cognitive symptoms during, but not between, attacks.

Deficits in spatial processing and memory are the most commonly investigated cognitive effects of vestibular dysfunction. This is because vestibular signals are used by the brain to create and recall mental representations of our location in, and movement through, space [Smith and Zheng, 2013; Mast et al., 2014; Yoder and Taube, 2014]. Across most analyses (including the whole sample and the subgroups of patients with peripheral disease and episodic vertigo, but not VM), patients had higher scores on the Space Perception subscale than controls (by 1.1–1.7 adjusted points). Scores on this subscale were correlated with the EMQ questions thought to be related to spatial memory or route-finding, although patients did not have significantly elevated scores on these question sets [Richardson and Chan, 1995; Cornish, 2000]. The results are consistent with prior studies showing objective deficits in spatial cognition in patients with vestibular loss [Brandt et al., 2005; Hufner et al., 2007; Kremmyda et al., 2016; Popp et al., 2017] and with studies measuring subjective reports of spatial difficulty. Similar to our results, Bisdorff et al. [2015] reported more difficulty on the “places” domain of the QAM in patients formally diagnosed with vestibular disease, and scores were correlated with ratings of vertigo symptoms. Likewise, Kremmyda et al. [2016] reported high levels of anxiety on the Spatial Anxiety scale, an 8-item questionnaire about situations that require spatial or navigational skills, in a small sample of patients with bilateral vestibular loss compared to controls. Although Lacroix et al. [2016] did not find elevated scores on the Space Perception subscale, this may be due to differences between a self-referred cohort (as in the Lacroix study) versus a formally diagnosed cohort (as in ours), or due to our use of covariates. The results support the notion that patients with vestibular disease have subjective difficulties with spatial cognition and suggest that the Space Perception subscale of the NVI is sensitive to these difficulties.

A smaller (but significant) difference between patients and controls was also found on the NVI Time Perception subscale for the whole sample and for patients with peripheral vestibular disease (0.8–1.0 adjusted points). This finding is interesting because there is evidence that similar cognitive processes are involved in orientation to space and time, and overlapping but distinct cortical areas (involving the inferior parietal cortex) have been identified [Walsh, 2003; Peer et al., 2015; Gauthier and van Wassenhove, 2016]. Behavioral studies suggest that people use spatial concepts and language to think about the more abstract construct of time [Boroditsky, 2000; Casasanto and Boroditsky, 2008; Parkinson et al., 2014]. It is therefore conceivable that diseases affecting spatial cognition may also affect the experience or representation of time. Alternately, perceptions of time may be impacted by more general effects of vestibular disease on attention.

Similar to Lacroix et al. [2016], we found that scores on the Memory subscale of the NVI were not elevated in any of the analyses; however, there was a trend for patients to report more memory problems than controls on the more comprehensive memory questionnaire, the EMQ. Only one previous study specifically investigated subjective impairment of memory in patients with vertigo, using the QAM, which has 62 questions about memory [Bisdorff et al. 2015]. The authors found that patients had more memory complaints than controls, in domains assessing “absentmindedness”; memory for “people,” “places,” “actions to be done,” and “facts of personal life”; as well as memory “in the presence of distracting factors.” Total scores on the QAM were correlated with patient reports of anxiety and depression (on the Beck Depression and Anxiety Inventories) and dizziness handicap (on the DHI), but not with the frequency of vertigo symptoms as assessed by the Vertigo Symptom Scale. The results are similar to those of the current study; however, patients’ memory complaints did not remain significantly elevated after controlling for the effects of psychological distress. Together, these studies suggest that patients with vestibular disease may not have significant memory complaints outside those related to psychological distress.

We conducted several additional analyses to investigate the specificity of cognitive complaints to different categories of patients. VM was the only formal diagnosis for which there were sufficient patients for individual comparison. These patients had significantly greater scores on the Attention subscale only. Patients with VM may be expected to have high levels of perceived cognitive dysfunction as migraine is primarily a disorder of the central nervous system. Migraine patients, with and without aura, report high levels of subjective cognitive dysfunction and psychological distress and show objective deficits during a migraine attack [Vuralli et al., 2018; Gil-Gouveia and Martins, 2019]. Our data do not enable us to distinguish between the effects of migraine headache and vertigo on cognitive complaints, or whether symptoms of cognitive dysfunction are temporally related to the vertigo or headache; however, Bisdorff et al. [2015] found that the presence of migraine per se was not related to subjective memory complaints.

The same analysis on patients whose cause of vertigo was located outside the central nervous system, in the vestibular organ or nerve, showed greater differences than control subjects. These patients reported difficulties with perceptions of space and time as well as attention. This is important as it demonstrates that the results are not unduly influenced by patients with a central cause of vertigo. It supports the studies in humans and animals with peripheral lesions of the vestibular system that show objective deficits in cognitive (mainly spatial) function [Smith and Zheng, 2013]. The findings were similar (except that there was only a trend toward a significant difference in the perception of time) when we grouped together patients with episodic vertigo caused by BPPV, VM, and MD, leaving out patients with chronic symptoms of vestibular loss. This is significant as nearly all prior research studies on cognition and the vestibular system have focused on patients (or animals) with a chronic loss of vestibular function, whether bilateral or unilateral, while most patients who attend neuro-otology clinics for dizziness and vertigo, and complain of “brain fog,” have episodic vertigo.

Taken together, our results suggest that patients with any disease of the vestibular system can experience heightened subjective levels of cognitive dysfunction compared to controls, in addition to the psychological distress that may accompany their illness. The common thread across the different vestibular diseases, many of which do not cause measurable damage to the vestibular organs or pathways, is a disturbance of the vestibular information relayed to the cortex, whether this is continuous or episodic. These changes can be expected to impact the higher centers in the brain which receive vestibular input, leading to potential alterations of the perceptions of motion and of “self-in-space” and memory for spatial information. As such, some of the cognitive complaints are likely to be directly produced by interruption of normal vestibular processing in the brain, such as those related to navigation and spatial memory. Others are more likely an indirect product of the vestibular disturbance, such as those related to attention and concentration. Finally, an important factor is the presence of an illness per se, as many diseases, especially chronic ones, have been associated with perceived cognitive decline due to their common effects on health and well-being [Wang et al., 2017; Jacob et al., 2019; Taylor et al., 2020].

Study Limitations

Our study had several limitations. While we included a relatively large sample of patients who were formally diagnosed with vestibular disease, there were insufficient numbers of patients with common diagnoses to warrant separate analyses. Future studies would benefit from larger sample sizes. Patients formally diagnosed with PPPD were underrepresented in this sample, although some of the patients with multiple diagnoses or no clear diagnosis at the time of classification had psychological symptoms, suggesting a potential role of PPPD. There may also have been some patients with PPPD who declined to participate in the study. Although we included a control group of nonvertiginous volunteers, it may be useful to compare vestibular patients to those with an alternate diagnosis, such as arthritis, to control for the general effects of chronic illness. As this was an exploratory study, we did not statistically correct for multiple comparisons, and future studies will be needed to verify the reproducibility of the results. While we asked patients directly if they thought they had cognitive issues as a result of their dizziness or vertigo, the NVI itself does not distinguish between recent changes in perceived function and long-standing cognitive weaknesses. Finally, an obvious limitation of this study is that we have measured only subjective reports of cognitive dysfunction. It is yet to be seen whether the presence of these symptoms translates to worse performance on cognitive tests [Crumley et al., 2014].

In summary, the results of our study show that cognitive dysfunction is a common subjective experience for patients with vertigo and dizziness. As many as 60% of patients in our neuro-otology outpatient sample attributed perceptions of cognitive dysfunction to their vestibular disease. The types of cognitive difficulties included problems with attention and concentration, and perceptions of space and time. The cognitive complaints were correlated with the high level of psychological distress experienced by patients, but mostly persisted after correcting for depression, anxiety, stress, and demographic factors. Defining the type and degree of cognitive issues experienced by patients represents an early step in addressing the potential objective cognitive effects of vestibular disease. Along with recognition of the emotional burden of vestibular disease, greater acknowledgment of the potential impact on cognition may be beneficial for affected patients.

We would like to thank Dr Emilie Lacroix for kindly providing us with the translated Neuropsychological Vertigo Inventory.

All participants gave written, informed consent according to the Declaration of Helsinki. The study was approved by the local Ethics Committee at Royal Prince Alfred Hospital (X13-0425 & X18-0097, HREC/18/RPAH/136).

The authors have no conflicts of interest to report.

This work was supported by the Neuro-Otology Society of Australia (NOTSA) and the National Health and Medical Research Council of Australia under Grant GNT1104772. Allison S. Young receives scholarship funding from the University of Sydney.

Danica Xie collected the data and edited the manuscript, Miriam S. Welgampola edited the manuscript, Laurie A. Miller critically revised the manuscript, Allison S. Young assisted with data collection and edited the manuscript, Mario D’Souza performed statistical analysis, Nora Breen edited the manuscript, and Sally M. Rosengren designed the study, supervised data collection, performed statistical analysis, and drafted and edited the manuscript.

The data that support the findings of this study are available from the corresponding author (S.M.R.) upon reasonable request.

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