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Original article

Postural control and sensory information integration abilities of boys with two subtypes of attention deficit hyperactivity disorder: a case-control study

Ren, Yuanchun; Yu, Lishen; Yang, Li; Cheng, Jia; Feng, Lei; Wang, Yufeng

Author Information
doi: 10.3760/cma.j.issn.0366-6999.20141559

Abstract

Attention deficit hyperactivity disorder (ADHD) is one of the most commonly diagnosed psychiatric disorder in childhood. In addition to the core ADHD symptoms of inattention, impulsiveness, and hyperactivity, these children are more likely to have neurological, developmental, learning, and interpersonal disorders than the typically developing peers, which make ADHD children to have a potentially poor prognosis.1 About 47%-69% of ADHD children have motor-coordination dysfunction.2,3 Children with the overlapping symptoms and signs of developmental coordination disorder have more serious neurodevelopmental, behavioral, psychosocial, and academic problems than children with ADHD only.4–6

However, few people pay attention to ADHD children's motor dysfunction and the existing researches show different findings. Denckla et al7 and Carte et al8 demonstrate that ADHD subjects are significantly slower than the controls in repetitive simple tasks of fingers, hands, and feet while Steger et al9 could not duplicate these findings in Finger-Tapping and Pegboard tests. Some researchers administer more complex tests, such as Movement Assessment Battery for Children and Bruiniks-Oseretsky Test of Motor Proficiency (BOTMP). Doyle et al10 determines that less than 10% ADHD-predominantly combined type (ADHD-C) children had motor skill difficulties during BOTMP. By contrast, Piek et al11 think boys with ADHD-predominantly inattentive type (ADHD-I) have significantly poorer fine motor skill while boys of ADHD-C experience significantly greater difficulty with gross motor skills. The discrepant findings may be resulted from subjective test biases and other interference effects, such as the subjects’ different age, gender, subtype, and taking of medicine or not.

Postural control is a fundamental function for human motor skill which requires the ability to integrate inputs from three sensory systems, i.e., somatosensory, visual, and vestibular. The technique of computerized dynamic posturography (CDP) has been applied widely in the clinical and laboratory research to objectively evaluate human's postural control function and the ability of sensory information processing.12,13 But few studies adopt CDP on ADHD children. Our research team reported there was static balance impairment in children with ADHD by using the instrument of Balance Master which adopted the skill of CDP.14–16 We could not answer how the three sensory system processing contributed to the postural control deficit limited by the technique at that time. Selina assessed 43 ADHD-C children's balance function adopting the SMART EquiTest and proposed that the visual system deficiency might be the reason for postural control disorder of the ADHD-C children.17 However, there was no discussion on the gender and subtypes which limit the result's explanation.

To sum up, the motor and sensory processing problems in children with ADHD are not well-studied. We suppose that there is developmental backward or defect on the posture control capacity of ADHD children compared with the normal control. And the different subtypes of children have different posture control performance. The problem of postural control may result from the damaged integration function in different degree of the three sensory information systems. To provide the neural physiological basis for non-pharmacologic measures and a better understanding of the clinical manifestations of ADHD, this study intends to compare standing balance function and analyze the sensory information processing ability between different subtypes of children with ADHD and typically developing children by using the technique of CDP in a large homogeneous sample controlling the gender and medicine treatment.

METHODS

Patients

Seventy-three boys between 7.6 and 15.3 years clinically diagnosed with ADHD and 73 normally developing controls matched by age, parents' economic status, and intelligence quotient (IQ) volunteered for this study between June 2003 and September 2004 (Table 1).

Table 1
Table 1:
Patient's characteristics

Boys with ADHD, comprising 49 boys with ADHD-I, 2 boys with ADHD-predominantly hyperactive/impulsive (ADHD-HI), and 22 boys with ADHD-C, were referred from the child psychiatric clinic at Peking University Institute of Mental Health. The control group was recruited from a common primary school and a high school.

Diagnoses of ADHD were made by two psychiatrists based on the American clinical diagnostic interview scales (CDIS). Control subjects had been neither evaluated nor treated for ADHD or any other developmental and behavioral problems.

Children were excluded if they have any of the following: (1) history of neurological conditions and neuropsychiatric diseases; (2) score of C-WISC lower than 85; and (3) significant musculoskeletal, cardiopulmonary, ocular, and otolaryngologic disorders which might influence the balance performance.

Ethics approval was obtained from the Institutional Review Board of Peking University Health Science Center, and all parents signed informed consent.

None of the ADHD subjects have been taking the prescribed medications for ADHD (i.e., methylphenidate, atomoxetine) before or during the study.

Measures

Postural control function was assessed by SMART EquiTest 8.0 (NeuroCom Int., Inc., Clackamas, OR, USA) instrument using static and dynamic CDP. The device consists of a dual force plate (rotation and translation capabilities), a movable visual surrounding, and a computer system. There are five sensors located in the four corners and the center of force plate which can measure the vertical forces exerted by the subjects' feet. CDP has been adopted as the only method to isolate the functional contributions of vestibular inputs, visual inputs, somatosensory inputs, central integrating mechanisms, and neuromuscular system outputs for postural and balance control18 and the instrument meets the testing standard for CDP set by the American Academy of Otolaryngology-Head and Neck Surgery and the American Academy of Neurology. The Sensory Organization Test (SOT) was used to evaluate the postural control and the contributions of different sensory systems to balance control. The procedures were conducted in a clinically routine fashion.19 Each subject received the measurement tested by one trained researcher.

During SOT, the subject stands on the force plate as quietly and steadily as possible. Six different conditions were used in order to examine the subject's balance control performance under different sensory conditions (Figure 1, Table 2). Each test condition was examined three times for 20 seconds with a 20-second break between tests.

Figure 1.
Figure 1.:
Six conditions (A-F) of SOT.
Table 2
Table 2:
Sensory input conditions during SOT

The comprehensive report includes the following: (1) Equilibrium score (ES): ES for each trial in each condition is calculated according to the formula:

where θmax(ant) is the maximum anterior sway angle during a trial; θmax(pos) is the maximum posterior sway angle during the same trial (negative); and 12.5 is the limit of sway degree in the sagittal plane for normal stance. The ES ranges between 0 and 100. Lower scores indicate increased body sway peak-to-peak amplitudes. The score of “0” was recorded if the subject falls, touches, or gripes reference for protecting. No body sway results in a perfect score of “100.” ES (1–6) is the average ES of all three trials in conditions 1–6.

The composite equilibrium score (CES) is evaluated as a weighted average of one subject's equilibrium scores from six conditions of the SOT: CES={ES(1)+ ES(2) +3[ES(3)+ ES(4) +ES(5)+ ES(6)]}/14.

(2) Sensory ratios:

The ability to use the three sensory systems (somatosensory, visual, and vestibular) to maintain postural control was evaluated by calculating the following ratios to identify impairments of individual sensory systems (Table 3).

Table 3
Table 3:
Computational formulas and the functional relevance of sensory ratio

(3) Strategy score:

The strategy score quantifies the amount of ankle and hip movement during each trial, calculated according to the shear forces of AP direction. The formula is: Strategy score={ 1-(SHmax-SHmin)/25}×100 where SHmax is the greatest horizontal AP shear force observed and SHmin is the lowest and 25 lbs is the average difference measured with a group of normal participants who use hip sway only to maintain balance on a narrow beam. Strategy score of each condition was the mean score of three trials and ranges between 0 and 100. A score approaching 100 indicated the subject predominantly used an ankle strategy to maintain equilibrium, while a score near 0 revealed the predominant usage of hip strategy.

Statistical analysis

All statistics were calculated with SPSS (version 13.0, SPSS Inc., Chicago, IL, USA). Paired-samples t-test and paired-samples Wilcoxon test (for abnormal distribution data) were used to compare the postural control function between boys with ADHD and the control group. One-way analysis of variance (ANOVA) and Kruskal-Wallis H test and Mann-Whitney U test (for abnormal distribution data) were employed for the overall mean comparison of the postural control function among the boys with ADHD-C and ADHD-I and the typical children. LSD and Dunnett's T3 methods were adopted, respectively, in multiple comparisons of inner groups to correct for type I error. The level of statistical significance was P <0.05.

RESULTS

Comparison of static postural control under various sensory input conditions between ADHD boys and the control group

Body sway

Compared with the control group, the ADHD group had a significantly lower CES and ESs in each condition (P <0.05) except condition 2 (Table 4). The boys with ADHD were more excited to the testing environment than the control and they had more sway of center of gravity even though the visual, vestibular, and somatosensory information were available. However, they could maintain balance by using the vestibular and somatosensory information when the visual inputs were missing (condition 2). It indicated that boys with ADHD had postural control problem in the condition that at least one kind of sensory information was removed and/or in conflict.

Table 4
Table 4:
Comparison of ES under six conditions between ADHD boys and the control group

Sensory ratios and strategy scores

Compared with the control group, the ADHD group had lower visual ratio and vestibular ratio (both P <0.05). It suggested that ADHD group had impaired abilities to use visual and vestibular inputs for maintaining balance. The strategy scores of ADHD boys were significantly lower than that of the control in conditions 4–6 (all P <0.05, Table 5) which indicated that, with the sensory input becoming increasingly insufficient or inaccurate, the ADHD group was more inclined to use the hip strategy for maintaining static balance than the control group. Additionally, in conditions 5 and 6, a score of “0” was recorded 27 times among ADHD boys, which was statistically much more than the “0” experienced 2 times by the control group (χ2=24.938, P <0.01). It showed that the vestibular system of the ADHD subjects failed to effectively integrate sensory information of insufficient and/or inaccurate visual or somatosensory perception, thus leading to loss balance.

Table 5
Table 5:
Comparison of sensory ratios and strategy scores between boys with ADHD and the control group

Comparison of postural control among boys of ADHD-I, ADHD-C, and controls

Body sway

Boys of ADHD-I had a significantly lower CES (P=0.003) and ES in conditions 4–6 than the control (P=0.0126, 0.043, 0.001), whereas ADHD-C boys had similar ESs as the ADHD-I boys in conditions 1–6; however, no significant difference was found between ADHD-C boys and control (all P >0.05, Table 6). These results indicated that ADHD-I boys experienced a greater body sway than the controls, and the disequilibrium became more evident when the sensory information inputs were insufficient, unavailable, or inaccurate. The postural control function of boys with ADHD-C had a trend behind that of the control.

Table 6
Table 6:
Comparison of ES under six conditions among boys with subtypes of ADHD and the control group

Sensory ratios and strategy scores

Compared with the control group, the ADHD-I boys showed significantly lower visual and vestibular ratios (P=0.011, 0.023), whereas the ADHD-C boys showed a trend of lower visual ratio than the control group (P=0.065). The ADHD-I boys had significantly lower strategy scores in conditions 4–6, while ADHD-C boys had similar strategy scores to ADHD-I and no significant difference was found between ADHD-C boys and control (Table 7). The ADHD-I boys had problem to use both visual and vestibular inputs for postural control and were more inclined to use the inefficient strategy (hip strategy) for maintaining static balance.

Table 7
Table 7:
Comparison of sensory ratios and strategy scores among boys with subtypes of ADHD and the control group

DISCUSSION

ADHD boys’ postural control function and abilities of sensory information processing

This study was to test and analyze the balance function and sensory information processing ability between different subtypes of children with ADHD and normal children using the technique of CDP in a large homogeneous sample controlling stimulants treatment. So the results can provide neural physiological evidences for the identification and treatment of motor problems of ADHD children.

First, we found the balance function of ADHD boys was generally weaker than that of normal boys. As the impairment may affect their participation in daily activities and increase the risk of injuries, this finding can explain the interesting phenomenon that ADHD children had higher rate of injury than their normal peers reported by surveys in several countries.20,21 Moreover, we found ADHD boys showed much more significant impairment of balance control with increasing task difficulty (i.e., reduction or conflict of sensory inputs) which is consistent with the earlier studies’ findings that ADHD children appeared to have motor impairment only in relatively complicated balance tasks in the presence of conflicting sensory inputs and dual-task walking.22,23

Postural control relies on the normal operation of sensory input, information integration, and musculoskeletal motion. Since the subject's nervous, musculoskeletal, ocular, and otorhinolaryngological diseases which might potentially affect the balance performance were excluded, the impaired balance performance of the ADHD boys can be attributed to deficits in the dysfunction of central nervous system's processing of sensory inputs. ADHD boys of this study have no problem to apply somatosensory inputs, which is consistent with the finding that the plantar pressure sensitivity of ADHD children was not lower than the normal control.24 So, a hypothesis was proposed that postural control dysfunction of ADHD boys was not because of the impairment in processing somatosensory inputs.

The most salient finding was that ADHD group had impaired abilities to use visual and vestibular inputs for maintaining balance. As we know, the visual function of a child matures at age between 7 and 10 years,25 and the ability to process inaccurate visual information develops after 13 years.26 Studies had proven the visuospatial impairment and visual-motor integration deficits in ADHD children.27,28 These findings support the hypothesis of delayed development in children with ADHD.29

Moreover, ADHD boys had a severe impaired vestibular information integration ability. The previous study of our team had evaluated the vestibular functions of 148 ADHD boys of 7–14 years of age.30 Their vestibular ocular reflex was normal, but their optokinetic nystagmus and visuo-vestibular ocular interactions were underdeveloped relative to normal subjects. It was considered that ADHD boys had no abnormality in the peripheral vestibular inputs but had defects in the central integration of conflicting information.

Our team also found ADHD children with lower vestibular scores, assessed by Sensory Integrative Scale, had severe impairments in suppression and planning ability.31 In another study we increased ADHD children's balance abilities and improved their cognitive functions (especially attention, memory, and response suppression) using Balance Master and EquiTest to train their vestibular system to integrate conflicting information.32 Vestibular system interacts with the visual cortex of the frontal lobe via visuo-vestibular interactions.33 The prefrontal cortex is implicated in executive functions including response suppression, attention, and non-distraction.34 The defects in information integration of vestibular central system may play an important role in the motor, postural control, and cognitive deficits of ADHD children. This study offers neurophysiologic clues for the incidence of ADHD and prompts a kind of potential non-drug treatment, which is vestibular information integration training.

Subtypes of ADHD boys’ postural control function and abilities of sensory information processing

We only analyzed the different performances of postural control between two subtypes of ADHD (ADHD-I and ADHD-C) and the control group as there were two boys with ADHD-HI which is not enough for statistical analysis. In contrast to the assumption that the motor problems and the subtypes of ADHD children were irrelevant since both ADHD-I and ADHD-C have similar balance performance as the control,35 we found only ADHD-I group had impaired postural control function, indicating that different subtypes of ADHD have different degrees of impairment in postural control. This finding can also be supported by the character of high clinical heterogeneity of children with ADHD and suggested that, of the three core symptoms of ADHD, attention deficit may be the one most closely related to postural control. An early developmental study reported that infants with abnormal postural control will experience difficulties in maintaining attention,36 suggesting the association between attention and postural control. Many dual-task studies37,38 revealed that the level of attention requires for maintaining balance varied with the task difficulty. The more difficult the balance task is, the more attention requires. We interpret these findings that postural control and attention share common neural pathways.

As to the comparison of information processing abilities, we found ADHD-C group showed a trend of impaired visual and vestibular information processing abilities compared with the control. It was considered that ADHD-C boys might compensate their compromised visual information utilization by the vestibular system. On the other hand, the small sample might be an interference factor. ADHD-I showed extensive and severe impairment in information processing than the control, which could be supported by the previous finding of Clark et al, that only ADHD-I of all the ADHD groups could benefit from vestibular training.39 According to a large number of clinical cases, Levinson40 pointed that functional impaired vestibular system cannot screen unnecessary stimulations, thereby resulting in difficulty of attention concentration or distraction easily by over-compensation. It means subject with impaired vestibular system should pay more attention to focus on the present work which would lead very easily to fatigue. To sum up, it was assumed that attention deficit is one manifestation of vestibular dysfunction. Barkley suggested that ADHD-I is attributed to impaired concentration or selection of attention while ADHD-C involves the problem of sustaining and allocation of attention. Accordingly, ADHD-I should be an independent subgroup of ADHD.34 Moreover, our study team assessed the vestibular function of 255 ADHD children by Child Sensory Integration Check Scale, and found ADHD children with vestibular dysfunction have more serious symptoms of hyperactivity and impulsivity and impairment of peer relationship and exhibit much more behavior problems, such as aggression disobedience and easily getting angry, than the group without vestibular dysfunction.41 Considering the significant performance variations of ADHD boys during posture control task of this study we propose that there are two other subtypes not reported previously, that is, ADHD with and without postural control dysfunction. Consequently, objective evaluation of postural control and sensory information processing in children with ADHD should be considered when clinicians make treatment plans. In view of the vestibular defection integrating conflict information being an important contributor to the clinical symptoms and cognitive deficits of ADHD-I children, the assessment and training of postural control under the condition of conflict and insufficient or inaccurate inputs should be introduced into the clinical diagnosis and intervention of ADHD children.

The limitations of small sample sizes need to be addressed. First, only two boys with ADHD-HI in this study may produce biased results. And the potential affects of comorbidities on the postural control ability could not be discussed. Moreover, due to the limited sample of ADHD-C, we found a trend of impaired information processing abilities in ADHD-C boys compared with the control. We hope to enlarge the sample size in a future study to further explore the characters of sensory information integration in boys with the three subtypes of ADHD.

In summary, we observed poorer static postural control ability and impaired function of processing visual and vestibular information in boys with ADHD, especially ADHD-I, compared with the normal control. The deficits may be an important contributor to the clinical presentation of ADHD children and their cognitive deficits. Assessment and training of postural control function would be suggested during the diagnosis and treatment of ADHD children.

Acknowledgements:

Appreciation is expressed to Dr. Owen Black, the director of Neurotology Research for Legacy in Portland for his assistance in the research. The authors also thank the participants and their parents for their contribution in this research.

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Keywords:

postural balance; sensory integration; attention deficit hyperactivity disorder; subtypes; childhood

© 2014 Chinese Medical Association