Neuropsychological profiles of children with vestibular loss

Abstract

BACKGROUND:

The impact of vestibular loss (VL) on cognition has been previously studied in experimental animal, human and adult patient studies showing links between VL, and cognitive impairments in space orientation, working memory, mental rotation and selective attention. However, few studies have been conducted on children with VL.

OBJECTIVE:

We investigated for the first time, the impact of a VL on children’s cognition.

METHODS:

13 children with VL (10 years, 5 months) and 60 average-age matched controls performed a neuropsychological assessment consisting of visuospatial working memory, selective visual attention, mental rotation and space orientation tasks.

RESULTS:

Children with VL recalled smaller sequences for both forward and backward memory subtasks (mean±SD = 6.3±1.9 and 5.3±2.6) than controls (8.2±2.3 and 7.3±2.0), have less accurate mental rotation scores (25.4±6 versus 30.8±5.1) and greater additional distance travelled in the maze task (96.4±66.6 versus 60.4±66.3); all corrected p-values <0.05. Selective visual attention measures do not show significant differences.

CONCLUSIONS:

Children with VL show similar cognitive difficulties that adults with VL, in tasks involving dynamic cognitive processes (higher attentional load) that in tasks requiring static cognitive processes such as visual attention task.

Keywords

Vestibular children neuropsychology cognitive abilities vestibular loss

1 Introduction

Vestibular loss (VL) in children is probably underestimated [45]. Very often, children do not have sufficient language abilities to complain of dizziness, and they lack a reference to understand that they have difficulty compared to others. These two problems associated with the fact that vestibular assessment is difficult to carry out in very young children, cause that VL in children is an “overlooked entity” [55].

In order to increase VL understanding in children, specifically adapted subjective measures have been recently developed. These include the Pediatric Vestibular Symptom Questionnaire (PVSQ) [36], the Pediatric Visually Induced Dizziness Questionnaire (PVID) [37] and the Dizziness Handicap Inventory - Pediatric (DHI-PC) [31]. The caregiver (or the child) carries all of these questionnaires out, and studies using these measures have shown good discrimination between children with vestibular symptoms and healthy controls. The addition of these new measures has brought increased understanding to the prevalence of VL in children; although, they do not measure potential associated cognitive difficulties.

On the contrary, adult studies of patients with VL have previously demonstrated specific subjective and objective cognitive impairments such as visuospatial working memory, mental rotation, attention, space orientation abilities, and/or a decrease in quality of life measures [1 , 49]. However, little is known about whether children have similar cognitive problems. The few studies that have been conducted on children with VL have tended to focus on the impact of VL on motor development, showing a global motor development delay [22 , 45] and/or an association of clumsiness and attention deficits [20]. Besides these results, the few studies that have investigated cognition in children with VL tend to show similar results to those of adult studies. For example, Beritoff (1965), demonstrated impaired navigation abilities in pediatric patients and in experimental animals with no detectable semicircular canal function [4]. Also, significant associations between vestibular dysfunction and poor performance at school have been reported [15, 56], indirectly suggesting a link between VL and cognitive development. One possible explanation to these altered school performances could be linked to a reduction of reading abilities due to an altered Dynamic Visual Acuity (DVA) [8, 46]. However, the specific cognitive processes that could be altered after a VL in children are still unknown.

As no previous studies have specifically investigated the neuropsychological profile of children with VL, we aim to create a study based on knowledge of cognitive deficits resulting from VL in adults. Based on this literature, we select four specific cognitive abilities that are classically impacted by VL in adults: (i) visuospatial working memory, (ii) mental rotation, (iii) selective attention, and (iv) space orientation. We will discuss each in the following four paragraphs.

Deficits in visuospatial working memory have been reported in experimental animals with VL [2 , 48], and in chronic bilateral patients with VL (bilateral VL, BVL), sometimes associated with a decreased hippocampal volume [7, 49]. For example, Popp et al. (2017) reported reduced performance for patients with VL relative to controls in two tasks measuring visuospatial working memory [40]. The first was the backward subtask of the Corsi Block Tapping Task (Wechsler, 1997), [53]. Here, the experimenter pointed to a series of blocks in a particular sequence and patients had to remember and point to the blocks in the reverse sequence order. Patients with VL on average remembered less of the sequence than control participants. This finding was in contrast to the forward subtask of the Corsi Block Tapping Task, where the patient had to remember the blocks shown by the experimenter in the same sequence order. In this subtask, there was no difference between patients with VL and control participants. Interestingly, we found a similar effect in adult patients with VL (data to be published), also only on the backward subtask from the Weschler Memory Scale (MEM-III, (Wechsler, 1997)). The second subtask was a whole report based on the Theory of Visual Attention (TVA-k) [14] where patients had to report as many letters as possible after seeing them on a computer screen. In this task, patients with VL reported less letters than controls. These two examples demonstrate that patients with VL may have impairments in visuospatial working memory.

Mental rotation (the ability to mentally rotate two or three-dimensional object images [50]) has also been found altered in adult patients with VL relative to controls [17 , 35]. However it is not clear which type of mental rotation is affected by the VL. For example, it has been shown that adult patients with BVL may be more affected by Egocentric Mental Transformation (EMT) involving the mental representation of one’s own body from the self-perspective (as if making an action) compared to Object-based Mental Transformations (OMT) where the object is imagined relative to the environment (as if observing someone else) [17 , 35]. On the contrary, Péruch et al. (2011) found an effect on OMT, where patients with bilateral VL suffering from Menière’s disease, tested before and after unilateral vestibular neurotomy, performed worse on 3-dimensional objects and in mental scanning of (un)familiar environments [38]. Therefore, these results may suggest some possible difficulties in performing mental rotation for patients with VL.

Selective attention (paying attention to a specific stimulus and inhibiting distractors) is also commonly reported as altered in adult patients with VL. Studies show evidence of both selective auditory and selective visual attention deficits using different tasks. For example, adult patients with unilateral VL (UVL) have been reported to have significant slower reaction times than control participants during an auditory choice inhibitory task where they had to respond as quickly as possible to a particular auditory target stimulus, and ignore distractor stimuli [41]. More recently, [40] reported that patients with VL showed slower reaction times than control participants for two tasks that involved selective visual attention. In the first task, patients had to report as many letters as possible in a column of five different red or green letters (TVA-c). In the second task, patients had to determine the presence (or not) of a critical target on a 5×5 matrix by quickly pushing one or another button (corresponding to target presence; yes/no), (Visual Scanning (TAP [58]).

Finally, space orientation (being able to relate position and positional changes of body or body parts to any stable reference system [33]) has been found to be altered in experimental studies on animals with VL and adult patients with VL. This ability is classically evaluated through real or virtual mazes where the animals/patients have to navigate around an environment. For example, in mutant mice without otoconia (the small calcium carbonate crystals included in the membrane covering the hair cells in the macula, the receptor organ of the utricle and saccule that provides gravisensor information) space orientation is altered in several types of mazes [28]. In adult patients with chronic BVL, space orientation has also been shown to be reduced relative to control participants in tests with a virtual variant of the Morris water task [7, 18]. Patients were worse than controls on this task, and they showed an hippocampus atrophy of 16.91% [7]. However, these structural changes were not found in other studies [11, 16]. As mentioned above, space orientation can also be measured through figure copying tasks, such as the Rey Complex Figure, [43]. Experimentation using Galvanic Vestibular Stimulation (GVS) has been reported to affect space orientation in stroke patients with visuo-spatial disorders when performing a copy of the complex 2-dimensional geometric Rey Complex Figure [57] whereby GVS modify patient’s copy performances, suggesting a link between vestibular system and the space perception and/or reconstruction of hierarchical visual form.

Based on this review, we aimed to explore these four cognitive functions in children with VL to determine whether they show similar impairments as adult patients with VL. However, one problem is to test children using equivalent measures to those used in adults, while motivating the children to complete the tasks. For visuospatial working memory, we decided to use the Corsi Block task from the Wechsler Nonverbal Scale of Ability (WNV, [54]) that is similar to the classical Corsi Block task commonly used in adults (including the forward and backward subtasks). As in the adult literature, we expect that children with VL should present more difficulty on the backward than forward subtask. For testing mental rotation, it is known that EMT tasks are more difficult (take more time) than OMT for children [21], so we propose to investigate mental rotation using a child-friendly well-validated OMT task, the puzzles from the NEPSY-II [25, 26]. We predict that children with VL will show a deficit in this task relative to control participants, being less accurate (making more errors). Selective attention can be tested with auditory or visual stimuli. However, as it is known that children with VL can have more frequently auditory associated disorders [10 , 52], we opted for a visual selective attention task. However, most of the adult visual selective attention tasks used in the literature are long and not suitable for children testing. We therefore used the cancellation faces test from the NEPSY-I [24]. This involves selecting target faces and ignoring distractor faces. Here we predict that children will make more errors and omissions that the control children. Finally, for evaluating space orientation, we selected the child-friendly “mazes 5–12” space orientation task [30]. The task involves visual perception, visuospatial working memory (as participants have to remember if they have already explored a path), and visual planning [30]. Here also, we predicted that children with VL would have more difficulties than controls (slower time or greater wrong directions).

2 Method

2.1 Participants

Thirteen patients with various VL were tested (Table 1) and compared to a group of sixty normally developed children. The groups did not differ in age (M = 10.5, SD = 3.9 years for patients and M = 10.7, SD = 3 years for controls; t(71) = 0.201, p = .841). Two control children did not complete all the testing due to technical issues, and the missing data (one for the memory task and one for the space orientation task) were excluded from the analysis. From the control participants, 53 self-reported being right-handed, 6 left-handed, 1 ambidextrous. For the patient group, 9 were right-handed, 3 were left-handed, and 1 was ambidextrous.

Table 1
Clinical data of the patients

Patients Laterality Sex PTAL PTAR Hearing Aid RC RW LC LW Asymmetry MCR oVEMP cVEMP

1 Right Male 41,25 2,5 None 35 31 30 19 15% / 1 1

2 Right Male 2,5 3,75 None 15 22 17 17 / 17,75 0 0

3 Right Female 15 8,75 None 5 10 15 9 23% / 0 1

4 Left Male 1,25 17,5 None 0 1,5 20 12 91% 8,375 n/a 0

5 Ambidextrous Male 41,25 21,25 UNI HA 22 21 34 21 12% / 0 1

6 Right Female 48,75 45 BI HA 9 22 11 32 16% / 0 1

7 Left Male 120 91,25 UNI CI 11 12 2 2 70% / 1 1

8 Right Male 15 36,25 UNI HA 0 6 8 19 64% / 0 2

9 Right Male 120 120 BI CI n/a n/a n/a n/a n/a n/a 0 1

10 Right Male 107,5 120 BI CI 0 n/a 2,7 n/a n/a 1,3 0 0

11 Right Male 15 8,75 None 0 0 11 25 100% / 0 1

12 Right Male 15 37,5 None 2,5 n/a 0,7 n/a n/a 1,5 n/a 0

13 Left Female 120 120 BI CI 0 8,4 6,9 0 / 3,825 1 0

Patients	Laterality	Sex	PTAL	PTAR	Hearing Aid	RC	RW	LC	LW	Asymmetry	MCR	oVEMP	cVEMP
1	Right	Male	41,25	2,5	None	35	31	30	19	15%	/	1	1
2	Right	Male	2,5	3,75	None	15	22	17	17	/	17,75	0	0
3	Right	Female	15	8,75	None	5	10	15	9	23%	/	0	1
4	Left	Male	1,25	17,5	None	0	1,5	20	12	91%	8,375	n/a	0
5	Ambidextrous	Male	41,25	21,25	UNI HA	22	21	34	21	12%	/	0	1
6	Right	Female	48,75	45	BI HA	9	22	11	32	16%	/	0	1
7	Left	Male	120	91,25	UNI CI	11	12	2	2	70%	/	1	1
8	Right	Male	15	36,25	UNI HA	0	6	8	19	64%	/	0	2
9	Right	Male	120	120	BI CI	n/a	n/a	n/a	n/a	n/a	n/a	0	1
10	Right	Male	107,5	120	BI CI	0	n/a	2,7	n/a	n/a	1,3	0	0
11	Right	Male	15	8,75	None	0	0	11	25	100%	/	0	1
12	Right	Male	15	37,5	None	2,5	n/a	0,7	n/a	n/a	1,5	n/a	0
13	Left	Female	120	120	BI CI	0	8,4	6,9	0	/	3,825	1	0

PTAL: Pure-tone hearing threshold average (frequencies 500–1000–2000–4000 Hz) for left ear; PTAR: Pure-tone hearing threshold average for right ear (dB). Hearing Aid: BI HA, bilateral hearing aid; UNI HA, unilateral hearing aid; BI CI, bilateral cochlear implant; UNI CI, unilateral cochlear implant. RC/RW/LC/LW: Averaged slow phase-speed for the right ear with cold water (30D°C) (RC) or warm water (44 D°C) (RW); left ear, cold (LC) or warm water (LW). oVEMP/cVEMP: Cervical/Ocular vestibular evoked myogenic potentials, (0 = absent bilaterally; 1 = absent or decreased unilaterally, 2 = Present). n/a: not available. MCR: Mean of the slow phase speed for the caloric response. Bold font is used to show pathological testing.

Patients were recruited through consultation for dizziness, balance disorders, clumsiness or other related learning difficulties in the Ear-Nose and Throat department of an academic hospital (**currently anonymized**). Vestibular loss was diagnosed after a medical examination performed by a senior ear, nose and throat physician on the basis of a video-nystagmography with bithermal water caloric irrigation (performed for the left and right ears at 44°C and 30°C), Cervical Vestibular-Evoked Myogenic Potentials (cVEMP) and/or Ocular Vestibular-Evoked Myogenic Potentials (oVEMP) (when possible). For the caloric testing and unilateral lesion, the difference of reflectivity between the ears was calculated using the Jongkees formula [(warm right ear + cold right ear) –(warm left ear + cold left ear)]/[(warm right ear + cold right ear + warm left ear + cold left ear)]×100 (expressed as a percentage) [19]. An asymmetry above 25% was considered pathological. For bilateral lesion, the mean of the slow phase speed was calculated (MCR). Through difficulties in testing children, our patient group showed a variety of completed clinical measures. Nevertheless, all patients showed at least one clinical test that was pathological. See Table 1 for the complete detailed clinical measures for each patient. Control participants were recruited using posters placed around the hospital, and through personal contacts.

Patient and control participants declared having normal or corrected vision, with no spontaneous nystagmus (verified by the senior ENT), neurological, psychiatric, or muscular disorders. The study was approved by the hospital ethics committee (see ClinicalTrials.gov Identifier: NCT02533739), and all procedures performed in the study were in accordance with the ethical standards of the institutional and national research committees, and with the 1964 Helsinki declaration and amendments. The testing session was approximately two hours, and breaks were provided throughout. The testing sessions were conducted in the ENT department of the academic hospital, or at the participant’s house.

2.2 Tasks

Visuospatial working memory was evaluated using the Corsi Block subtask of the Wechsler Nonverbal Scale of Ability (WNV, [54]). Ten blue blocks were presented on a white board in front of the children. The examiner touched a series of blocks sequentially, and asked the children to repeat the sequence by touching the same blocks in the same order (forward span), or in the reverse order (backward span). The number of blocks in the sequence was systematically increased across trials for each task order (i.e., the forward span was conducted at a different time then the backward span). The task was stopped when the child failed to correctly recall a sequence of the same level on two consecutive occasions. The measures were the maximum span achieved in the forward and backward condition. Additionally, the span difference between the forward and backward subtask was walculated in order to investigate if our patient group showed a larger difference relative to the control group (with more difficulty on the backward task).

Mental rotation (OMT) was evaluated using the subtask “Geometric Puzzles” from the NEPSY-II, [25, 26]. In this task, the children viewed a picture of a grid that contained several shapes. The participant had to match two shapes outside of the grip with two shapes within the grid. To perform the task, the participant had to mentally rotate the pieces of the geometrical puzzles in order to determine if they belonged to the presented item or not. The final score expressed the number of succeeded items.

Selective visual attention was tested using the faces cancellation subtask from the NEPSY-I [24]. Children were asked to pay attention to two drawings of a woman and a man’s face, and then to cancel the maximum number of identical faces that they could find amongst other similar faces linearly arranged on an A3 sheet of paper. The non-identical other faces shared some characteristics with the target faces such as a smile, same eyes or same hair. The children were given a maximum of 180 seconds to perform the task. Three measures were recorded: the total numbers of omissions (TO), the total number of errors when incorrect faces were selected (TE) and reaction time to complete the task (RT) (if the child succeed to complete the task before 180 sec).

Space orientation was evaluated with the task “Mazes 5–12” [30]. In this task, several mazes of increasing complexity were given to the children with different characteristics of dimensions: square/round, and with thin or bold lines. The recorded measures were average total time to complete the succeed mazes (TT), the average total number of cut lines where the child crossed over a barrier line in the maze (CL), the average total number of wrong directions made when performing the task (WD), and the average travelled distance (DA).

2.3 Procedure

Before each experiment, participants and their parents received information about the study, they confirmed their consent, and they responded to demographic questions. This was followed by the randomly presented neuropsychological measures. The study was performed in a single session, with except for two participants where the tasks were performed in two separate sessions.

2.4 Statistical analysis

As the sample sizes of the groups were different, and normality assumptions were violated several time, as verified with the Kolmogorov- Smirnov test, nonparametric Mann-Whitney U tests were used for testing differences between groups. The adjusted p values were added following Benjamini–Hochberg (1995), [3] to take into account the false discovery rate.

3 Results

For the visuospatial working memory task, patients recalled smaller sequences for both forward and backward subtasks (mean±SD = 6.3±1.9 and 5.3±2.6 respectively) compared to controls (8.2±2.3 and 7.3±2.0) (original and adjusted p-values all <0.05, conforming to Mann–hitney U tests after Benjamini–Hochberg correction). Span difference (between forward and backward subtasks) was not significant (original and adjusted p-value >.05). In the mental rotation task patients were significantly less accurate (mean±SD = 25.4±6) than the control group (mean±SD = 30.8±5.1) (original and adjusted p-values all <0.05). In the selective visual attention Faces cancellation task there was no significant differences between the two groups (original and adjusted p-value >0.05). The space orientation maze task showed a significant difference between groups for the dependent variable of additional distance travelled, with the patient group demonstrating a greater additional distance travelled (mean±SD: 96.4±66.6) than the control group (mean±SD = 60.4±66.3) (original and adjusted p-value <0.05). Other parameters revealed no significant differences. See Table 2 for detailed scores.

Table 2
Detailed scores for the vestibular cognitive tasks for patients and control group

Cognitive function Measures Patient group* M (SD) Control group* M (SD) Mann-Whitney U (p-value) Adujsted p¹

Visuospatial working memory WNV –Forward span 6.3 (1.9) 8.2 (2.3) 0.005 0.027

WNV –Backward span 5.3 (2.6) 7.3 (2.0) 0.012 0.038

Span differences 1 (1.8) 0.9 (1.7) 0.804 0.804

Mental Rotation NESPY II –Geometric Puzzles 25.4 (6.0) 30.8 (5.1) 0.002 0.022

Selective Visual Attention NESPY I –Faces cancellation –TO 3.9 (2.9) 2.9 (3.0) 0.115 0.253

NESPY I –Faces cancellation –TE 1.3 (1.9) 0.6 (0.9) 0.167 0.262

NESPY I –Faces cancellation –RT (sec) 149.0 (29.5) 151.2 (30.8) 0.690 0.759

Space orientation Mazes 5–12 –TT (sec) 588.1 (236.1) 492.0 (128.8) 0.141 0.258

Mazes 5–12 –CL 23.9 (23.8) 16.5 (18.8) 0.244 0.335

Mazes 5–12 –WD 10.2 (6.8) 8.4 (6.4) 0.366 0.447

Mazes 5–12 –DA 96.4 (66.6) 60.4 (66.3) 0.014 0.038

Cognitive function	Measures	Patient group* M (SD)	Control group* M (SD)	Mann-Whitney U (p-value)	Adujsted p¹
Visuospatial working memory	WNV –Forward span	6.3 (1.9)	8.2 (2.3)	0.005	0.027
	WNV –Backward span	5.3 (2.6)	7.3 (2.0)	0.012	0.038
	Span differences	1 (1.8)	0.9 (1.7)	0.804	0.804
Mental Rotation	NESPY II –Geometric Puzzles	25.4 (6.0)	30.8 (5.1)	0.002	0.022
Selective Visual Attention	NESPY I –Faces cancellation –TO	3.9 (2.9)	2.9 (3.0)	0.115	0.253
	NESPY I –Faces cancellation –TE	1.3 (1.9)	0.6 (0.9)	0.167	0.262
	NESPY I –Faces cancellation –RT (sec)	149.0 (29.5)	151.2 (30.8)	0.690	0.759
Space orientation	Mazes 5–12 –TT (sec)	588.1 (236.1)	492.0 (128.8)	0.141	0.258
	Mazes 5–12 –CL	23.9 (23.8)	16.5 (18.8)	0.244	0.335
	Mazes 5–12 –WD	10.2 (6.8)	8.4 (6.4)	0.366	0.447
	Mazes 5–12 –DA	96.4 (66.6)	60.4 (66.3)	0.014	0.038

TO: The total numbers of omission; TE: The total numbers of errors; RT: reaction time; TT: Total time (for succeed mazes); CL: total cut lines; WD: Total wrong directions; DA: Additional travelled distance. ¹p value adjusted according to Benjamini–Hochberg (1995). *n = 13 for the patient group, n = 60 for the control group except for visuospatial memory and space orientation where n = 59).

4 Discussion

The objective of the present research was to explore the cognitive abilities impacted in children with VL using child-friendly tests. More precisely, based on the adult and animal literature, we selected four cognitive dimensions to assess: visuospatial working memory, mental rotation, selective visual attention and space orientation. Our results showed evidence for some cognitive problems in children with VL compared to average-age matched controls. Although our patient sample presented heterogeneous vestibular profiles, with some patients having possible remaining canalar or otolithic vestibular function, the results were consistent with existing adult literature showing that visuospatial working memory [7, 40], mental rotation [17, 38], and space orientation abilities [7, 18] were reduced for adult patients with VL compared to control participants at the group-comparison level. To our knowledge, this is the first time that specific cognitive impairments have been measured in children with VL. However, our analyses are clearly limited by the variability of the vestibular loss and the presence of concurrent hearing loss.

The absence of differences between children with VL and control group for selective visual attention task could be due to the task choice for the study. Indeed, our tasks were selected based on the adult VL literature combined with the presence of well-validated and easy to use child-friendly tasks. For example, the faces cancellation task used in our study was designed to evaluate selective attention by measuring accuracy (errors/omissions), whereas the attentional deficits shown in adult with VL mostly concerned response time in computerised tasks [40, 41]. These last tasks measuring visual attention could also potentially involve other abilities such as sustained attention due to the task length. These differences in tasks could partially explain the lack of significant difference between our children with VL patient group and controls.

On the basis of our results, we discuss two other hypotheses that might explain our findings, and could be taken into account in future studies. These hypotheses explain the results from the perspectives of task solving processes or the associated cognitive demands of tasks.

Concerning the solving process required, our tasks could be split into two groups based on their static (for faces cancellation) or dynamic (for visuospatial working memory, mental rotation and mazes tasks) characteristics. This distinction between dynamic and static cognitive processes has been previously described by Pickering et al. (2001) [39]. They reported that children showed different developmental patterns in a static matrix task (i.e., where the children had to remember a pattern of fixed black squares in a matrix on a computer screen) versus a dynamic matrix task (i.e., where the children had to recall the location and order of a series of black squares presented one at a time on a computer screen) [39]. Although this distinction between static and dynamic process was originally designed for the modality of the task presentation, this definition could be extended to the cognitive processes required to solve it (and not only the presentation modality). For example, dynamic tasks could involve a “mental movement” during their execution to solve the task (such as in mental rotation). On the contrary, static task would not involve mental movement (such as when performing a target detection task).

For the three tasks in our study that showed significant differences, this mental movement (dynamic process) during task execution is present. In the Corsi, the children have to see the experimenter’s movements and have to remember this movement (dynamic) mentally to reproduce it. In the mental rotation, a mental movement is required to solve the task. Finally, in the mazes, a virtual mental movement/displacement seems to be necessary in order to correctly draw the path in the task. On the contrary, for the remaining task (Faces cancellation), the targets were fixed and no mental movement was required to execute this task. The faces cancellation requires arm and hand real movement to cancel the target but no mental movement representation as the targets are always present on the sheet of paper. Future studies could try to assess the difference between static and dynamic tasks by either using task that requires these different processes and or combining these measures with subjective questionnaires that allow to ensure the participants solving strategy.

Concerning the associated cognitive demands hypothesis, some of the tasks that we used in this study could require more cognitive abilities than others. For example, a cancellation task does not require visuospatial working memory while a mental rotation task on the contrary does [6 , 21]. Also, visuospatial working memory requires a proper development of the executive function network [32, 51]. Furthermore, the level of cognitive resources required for one task would vary with age as, for example, the maturation of executive function appears between 6 and 8 years [12 , 47], making highly complicated to measures the associated cognitive demands of each task. In our study, this alternative explanation could partially explain why the faces cancellation task does not show any significant group difference, as this is a more basic target-detection task that would require less cognitive demands. Unfortunately, the small sample size used in our study does not allow to drive definitive conclusions for this task and more children studies with larger sample sizes are required to investigate the role of the associated cognitive demands. Furthermore, complementary vestibular measurements such as the video head impulse test (VHIT) may provide additional information that allows a deeper understanding of the links between verstibular function and cognition, particularly for high frequency responses.

Finally, future studies should pay particular attention to children with VL with concurrent hearing loss. As with the majority of single centre clinical studies, our patient sample had a large heterogeneity in the degree of vestibular and hearing loss. The different asymmetry of hearing experience in these children, and the presence or absence of unilateral/bilateral hearing aid or cochlear implant may have influenced the cognitive profile of the patients. For example, it has previously been demonstrated that the gross motor trajectory development can be changed in children with hearing loss after a cochlear implantation [23] with possible associated cognitive impairments. Although the heterogeneity and the size of our sample does not allow proper group comparison taking into account the hearing loss and the type of hearing aid, we propose that, in addition to the systematic vestibular physiological assessment, a cognitive neuropsychological assessment should always be performed for these children, with a particular attention to visuospatial working memory, mental rotation and space orientation.

4 Compliance with ethical standards

4.1 Conflict of Interest

All authors have no conflicting interests to report.

4.2 Ethical approval

The research procedures were in accordance with the ethical standards of the institutional and national research committee, and in accordance with the 1964 Helsinki declaration, and subsequent amendments (Clinical-Trial-Number NCT02533739). Informed consent: Informed consent was obtained from each individual participant, and their parents prior to any participation in the study.

Footnotes

Acknowledgments

This study was funded by the Saint-Luc hospital Foundation (no grant number). The authors would like to thank the members of the E.N.T. department and the Center of Audiophonology, both at Cliniques Universitaires Saint-Luc for their comments and feedback, and all the participants who took part in the study. The authors have stated that they had no interests which might be perceived as posing a conflict or bias.

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