Cerebral palsy (CP) is the most common cause of childhood physical disability, with a prevalence of more than 1 in 700 (Australian Cerebral Palsy Register, 2020; Smithers-Sheedy et al., 2016, 2018; Stavsky et al., 2017). Although clinical interventions frequently focus on the physical difficulties experienced by children with CP (Bodimeade et al., 2013), the early disruptions in brain development are associated with a range of attentional, behavioural and executive function difficulties (Crichton et al., 2020; Fluss & Lidzba, 2020). Attentional and behavioural disorders, executive function deficits and autism spectrum disorder occur more frequently in children with CP than in the general population (Bodimeade et al., 2013; Craig et al., 2019; Påhlman et al., 2019; Warschausky et al., 2017). Increasingly, attention is focused on these associated neurodevelopmental challenges, and their impacts on everyday functioning (Bottcher et al., 2010), with researchers indicating a need for detailed studies of such impairments in children with CP (Craig et al., 2019; Påhlman et al., 2019). Further, clinical guidelines highlight the importance of screening for such neurodevelopmental difficulties in this population (National Guideline Alliance, 2017). This population-based cohort study aimed to assess attention, executive function and autism symptomatology using parent-report measures designed to give insight into everyday functioning. It also aimed to explore what impact gross motor function has on prevalence of these neurodevelopmental differences in children with cerebral palsy.

Executive Functioning

Executive functioning (EF) refers to higher order cognitive abilities and processes associated with deciding on, planning and working towards goals (Piovesana et al., 2015; Warschausky et al., 2017), regulating emotions and behaviour (Diamond, 2013), and responding flexibly in the face of changing situations or difficulties (Sørensen et al., 2016). As executive functioning skills are key in all parts of daily life, including health, academic and vocational achievement (Diamond, 2013), participation (Bottcher et al., 2010), and adaptive functioning (Warschausky et al., 2017), impact of impaired EF can be wide-ranging.

As a psychological construct, there have been challenges with how best to define EF (Zelazo & Müller, 2010). Zelazo and Müller (2010) consider EF from a developmental perspective, and suggest a problem-solving framework for understanding the concept, rather than listing different components of EF, or envisoning an overarching cognitive ‘module’. As development progresses, and the activities - and problems - of daily life increase in complexity, so do more sophisticated EF skills emerge. Zelazo and Müller (2010) note important changes in EF can occur between the ages of two and five, such as early planning and regulation abilities, while some aspects of EF continue to develop throughout adolescence and into early adulthood (Best & Miller, 2010; Sørensen et al., 2016). For example, cognitive flexibility, the ability to take alternative perspectives and adapt to changing demands, is thought to emerge later in adolescence (Diamond, 2014).

A 2013 systematic review found that across six studies, all domains of EF were poorer in children with CP than in typically developing children (Weierink et al., 2013). In 2010, Bottcher et al. reviewed cognitive functioning in children with spastic CP and reported that limited research on attention and EF in CP meant that no general picture was available for how these domains develop in children with spastic CP. The authors noted that it could not be determined whether difficulties with attention and EF were due to developmental delays or permanent impairment (Bottcher, 2010). A developmental perspective on the emergence of executive functioning abilities, such as proposed by Zelazo and Müller (2010), can assist with understanding how a non-progressive injury to the infant brain, as occurs in CP, may continue to impact developmental trajectories of individuals at different stages of their life. Insight into patterns of EF dysfunction in children with CP at different stages of development is key to furthering this understanding.

Attention and Hyperactivity/Impulsivity

Attention encompasses a wide range of cognitive mechanisms, including the ability to ignore irrelevant stimuli (selective attention), to sustain concentration or performance over time (sustained attention) or the ability to perform more than one task at a time (divided attention) (Cohen, 2011; Hommel et al., 2019). In terms of developmental disorders, deficits in attention are most characteristically associated with attention deficit hyperactivity disorder (ADHD), which may present as predominantly inattentive, predominantly hyperactive/impulsive or as a combined presentation (American Psychiatric Association, 2013, 2022; Biederman, 2005). For the hyperactive/impulsive presentation, key features are excess motor activity, fidgeting and poor control of impulses (American Psychiatric Association, 2022). ADHD in childhood can be associated with academic and social difficulties, while adolescents and adults with ADHD are at higher risk of ongoing academic difficulties, substance abuse, poor self-esteem, psychosocial disadvantage, and mental health concerns (Biederman, 2005). For all presentations of ADHD, emotional dysregulation is much more common than in the general population, and can further contribute to challenges with peer and family relationships, participation in daily life, and academic and vocational functioning (Shaw et al., 2014). A systematic review of comorbidity between CP, ASD and ADHD found that for 1795 children and adolescents in studies that explored the co-occurrence of ADHD with CP, 22% of participants met criteria for ADHD (Craig et al., 2019), compared to 7% of typically developing children (American Psychiatric Association, 2022).

Autism

Autism spectrum disorder (ASD) is characterised by deficits in social interaction along with the presence of restricted and repetitive behavioural patterns, activities or interests (American Psychiatric Association, 2022; Lord et al., 2018). ASD prevalence in the general population is around 1% (American Psychiatric Association, 2022; Craig et al., 2019), and while estimates of the male-to-female ratio vary, prevalence in males has been consistently found to be greater (Lord et al., 2018), with one systematic review estimating it to be 3:1 (Loomes et al., 2017). Children with CP are considered to be at higher risk of being diagnosed with ASD, with a recent systematic review of comorbidity in children diagnosed with CP reporting prevalence rates from 2 to 30% across 16 studies (Craig et al., 2019).

Assessment Considerations

Assessment of executive functioning and attention presents some challenges, given the diversity of cognitive processes involved (Pereira et al., 2018). Measures can be divided into performance-based tasks and ratings measures, with respondents completing scales or questionnaires (Warschausky et al., 2017). While performance-based tasks can assess specific functions, such as working memory or inhibition, ratings measures or questionnaires can provide insight into executive functioning in daily life (Pereira et al., 2018). Previous research has found ratings measures to be better at discriminating between children with attentional disorders and typically developing peers (Davidson et al., 2016). Motor and speech impairments may impact the validity of assessment measures when working with children with CP (Craig et al., 2019). Ratings measures completed by parents and teachers may avoid to an extent the impact of motor and/or speech impairments on performance-based testing. However, it is noted that rating measures are still impacted by motor and communication challenges of the individuals being assessed, due to issues with the applicability of items on the scale. As a result, this study does not include any participants at GMFCS level V.

This population-based cohort study aimed to assess attention, behaviour, executive function and autism symptomatology in school-aged children diagnosed with CP using parent-report measures designed to provide insight into everyday functioning. The study included a sample of the CP population of school-aged children with a distribution of functional severity similar to that in an Australian population sample (Australian Cerebral Palsy Register Group, 2018) across GMFCS levels I-IV. As well as exploring outcomes across these areas of neurodevelopmental functioning, the study explored relationships between functional capacity (GMFCS) and outcomes on measures of attention and behaviour, and executive function, and between sex and autism symptomatology.

Method

Study Design

This study analysed cross-sectional data from a prospective population-based cohort study, Predict-CP (an NHMRC 1077257 Partnership Project: Comprehensive surveillance to PREDICT outcomes for school age children with CP (Boyd et al., 2017). 

Ethics

Ethics approval for the Predict-CP study was given by Children’s Health Queensland Hospital and Health Service Human Research Ethics Committee (HREC/14/QRCH/329) and the University of Queensland’s Human Research Ethics Committees (2014001487).

Participants

Participants were children diagnosed with CP born between January 2006 and December 2011 and living in Queensland, Australia. State-wide recruitment, in collaboration with the Queensland Cerebral Palsy Register and the Queensland Paediatric Rehabilitation Service, was undertaken, with a recruitment sample for the birth years of n = 248 by the age of 5 years. Of these families contacted when their child was 8–12 years, 93 consented and attended for assessment, while 46 did not respond to invitations to participate, 44 declined, 32 were ineligible, 27 were lost to follow-up, and 6 were deceased. Eligible participants and their parents or caregivers attended the Child Health Research Centre, Brisbane, Australia, for assessment. Informed consent was obtained from caregivers and participants and demographic data were collected. Participants were included in this study when data for the relevant assessment measures were available. A registered psychologist conducted the assessments reported in this study.

Measures

A comprehensive assessment protocol was developed to gain insight into neurodevelopmental outcomes for school-aged children with CP (Boyd et al., 2017). Parents completed measures of attention and behaviour (Conners-3 Parent short form), executive function (Behaviour Rating Inventory of Executive Function – BRIEF) and autism symptomatology (AQ-10 – Child version). Participant scores on the Raven’s Coloured Progressive Matrices (RCPM) were used to control for cognition. The RCPM was chosen as part of the broader study protocol as it can be used with participants with motor and/or communication challenges. Administration was modified for a participant who used Augmentative and Alternative Communication (AAC). Instead of pointing to or stating the answer, the participant answered ‘yes’ or ‘no’ via their AAC device as the assessor pointed to each option.

Raven’s Coloured Progressive Matrices

(RCPM) is a 36-item measure of nonverbal intelligence for children aged 5–11 years (Pueyo et al., 2008; Raven & Court, 1998). After viewing a matrix, children are required to select a piece that will best complete the matrix. In a study of Australian children aged 6–11, the RCPM showed good internal consistency (0.76–0.88) and split-half reliability (0.81-0.090) (Cotton et al., 2005).

The Conners-3 Parent Short Form (Conners-3)

assesses for attention deficit hyperactivity disorder (ADHD) and behavioural and emotional disorders in children and adolescents aged 6–18 years (Conners, 2008). It measures inattention, learning problems, aggression, family relations, hyperactivity/impulsivity, executive functioning and peer relations. The short form has been found to be a valid tool to assess for ADHD (Izzo et al., 2019). Parents or guardians rate statements using a four-point scale ranging from ‘0, not true at all (never, seldom)’ to ‘3, very much true (very often, very frequently)’. On the Conners-3, higher scores indicate higher levels of concern. T-scores from 65 to 69 are considered clinically elevated. T-scores at or above 70 are considered very elevated. Internal consistency (α = 0.85–0.92) and test–retest reliability (r = .73–0.97) are sound for the Conners-3 Parent Short-form version (Conners, 2008).

The Behaviour Rating Inventory of Executive Function (BRIEF)

assesses the child’s executive functioning in everyday life. The BRIEF is an 85-item parent-rated questionnaire assessing behavioural manifestations of executive functions in everyday life (Gioia et al., 2002). The BRIEF produces a Behavioural Regulation Index (BRI; Initiate, Working Memory, Plan/Organise, Organisation of Materials, and Monitor subscales), a Metacognition Index (MCI; Inhibit, Emotional Control, and Shift subscales), and a Global Executive Composite. The BRIEF has been shown to be a valid measure of executive functioning and has good internal consistency (α = 0.80–0.98) and high test-retest reliability on the BRI (r = 0.92), MCI (r = 0.88), and the GEC (r = 0.86) (Gioia et al., 2002). While a newer edition has since been published, it was not available at the time the protocol was determined for the current study.

The Autism Spectrum Quotient – Child Version (AQ10-Child)

is a 10-item autism screening measure based on parent report for children aged 4–11 years (Allison et al., 2012). For the child version, using a cut-off point of six, the scale has a high internal consistency (Cronbach’s α = 0.90), while positive predictive value is 0.94, sensitivity is 0.95, and specificity is 0.97 (Allison et al., 2012; Boyd et al., 2017).

Statistical Methods

Data analysis was performed using SPSS Statistics Version 27. Variables were screened for missing data, outliers, and normality. Some outcomes included slightly reduced sample numbers due to the inability of some participants to complete all components of the protocol. Numbers in tables indicate the impacted scales. Analysis was via one-sample t-tests, comparing against population means from normative samples, along with MANCOVAs to determine group differences based on GMFCS level after controlling for cognition. Cognition was controlled for using scores from the RCPM, with scores ≤ 70 considered to be well below expected for the participant’s age. EF domains measured were behavioural regulation, metacognition and global executive composite. Behavioural subscales were inattention, hyperactivity/impulsivity, learning problems, EF, defiance/aggression and peer relationships. Finally, to account for multiple comparisons, tests were considered significant at a Bonferroni-adjusted p-value of < 0.008.

Results

74 participants (male n = 51) mean age 9 years 9 months, SD 1 year 1.2 months (range 8 years 0 months to 12 years 11 months), GMFCS I = 45 (60.8%), II = 17 (23%), III = 8 (10.8%), and IV = 4 (5.4%), were assessed on measures of attention (Conners-3 Parent short form), executive function (Behaviour Rating Inventory of Executive Function – BRIEF) and autism symptomatology (AQ-10). Pearson’s chi-square tests of contingencies were used to determine if those who participated in the study differed significantly from the overall recruitment sample. No significant differences emerged for sex, presence of epilepsy, GMFCS level, motor type or prematurity. Participant characteristics are displayed in Table 1.

Table 1 Characteristics of Participants (N = 74)
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Attention

Results of one-sample t-tests comparing the performance of study participants against population means for Inattention, Hyperactivity/Impulsivity, Learning Problems, Executive Function, Defiance/Aggression and Peer Relations subscales are displayed in Table 2. The study sample differed significantly from the population mean across all domains. Greatest impairment was reported on the Peer Relations (M = 72.7, SD = 16.2, t(73) = 12.0, p < .001) and Inattention (M = 66.3, SD = 12.5, t(73) = 11.2, p < .001) subscales, but results were also statistically significant for Hyperactivity/Impulsivity (M = 64.0, SD = 13.5, t(73) = 8.9, p < .001); Learning Problems (M = 66.1, SD = 13.5, t(73) = 10.2, p < .001); Defiance/Aggression (M = 57.3, SD = 13.5, t(73) = 4.6, p < .001); and Executive Function (M = 60.9, SD = 12.0, t(73) = 7.8, p < .001).

Table 2 Conners-3 Attention Scores in Children with CP Compared with Population Means (M = 50, SD = 10)
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Participants’ scores could also be classified by range in the domains of Inattention and Hyperactivity – scales related to presentation types of ADHD. On the Conners-3, T-scores from 65 to 69 are considered elevated, while T-scores at or above 70 are considered highly elevated. For the Inattention content scale, 50.7% of the sample scored within the Elevated to Very Elevated range. For Hyperactivity/Impulsivity, 46.7% of the sample scored within the Elevated to Very Elevated range. For both domains, the percentage of male participants falling within the Elevated to Very Elevated range was higher than the percentage of female participants. For Inattention, 53.8% of males fell within the Elevated to Very Elevated range, compared with 43.5% of females. For Hyperactivity/Impulsivity, 50% of males scored within the Elevated to Very Elevated range, compared with 39.1% of females.

In order to explore attention and behaviour while controlling for cognitive ability, the performance of study participants who scored above 70 on the RCPM was compared to population means for all content scales of the Conners-3. The study sample differed significantly from the population mean across all domains on one-sample t-tests. Greatest impairment was again reported on the Peer Relations (M = 71.0, SD = 16.6, t(48) = 8.9, p < .001) and Inattention (M = 63.1, SD = 11.9, t(48) = 7.7, p < .001) subscales, but results were also statistically significant for Hyperactivity/Impulsivity (M = 61.3, SD = 12.6, t(48) = 6.3, p < .001); Learning Problems (M = 61.2, SD = 11.9, t(48) = 6.6, p < .001); Defiance/Aggression (M = 55.6, SD = 12.3, t(48) = 3.2, p = .001); and Executive Function (M = 58.9, SD = 11.1, t(48) = 5.6, p < .001).

Executive Function

The performance of study participants compared to population means for Inhibit, Shift, Emotional Control, Initiate, Working Memory, Plan/Organise, Organisation of Materials and Monitor subscales, as well as the Behavioural Regulation Index, Metacognition Index and Global Executive Composite are reported in Table 3. The study sample differed significantly from the population mean across all domains on one-sample t-tests, with the Working Memory subscale the domain where participants differed most from the population mean (M = 60.7, SD = 10.0, t(72) = 9.2, p < .001), closely followed by the Shift subscale (M = 60.4, SD = 12.7, t(72) = 7.0, p < .001).

Table 3 BRIEF Measures of Executive Function in Children with CP Compared with Population Means (M = 50, SD = 10)
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In order to explore executive function while controlling for cognitive ability, the performance of study participants who scored above 70 on the RCPM was compared to population means for all subscales of the BRIEF, as well as the Behavioural Regulation Index, Metacognition Index and Global Executive Composite. Results are reported in Table 4. The study sample differed significantly from the population mean across all domains on one-sample t-tests. The Shift subscale was the domain where participants differed most from the population mean (M = 58.4, SD = 11.8, t(47) = 4.9, p < .001), followed by the Working Memory Subscale (M = 57.9, SD = 8.3, t(47) = 6.6, p < .001.

Table 4 BRIEF Measures of Executive Function in Children with CP Compared with Population Means for Participants with RCPM scores > 70 (M = 50, SD = 10)
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Autism Symptomatology

On a screening measure of autism symptomatology, 27 participants (29.1%) scored at or above the clinical cut-off at which referral for full autism assessment is recommended. To evaluate whether sex was related to reported autism symptomatology, a Pearson’s chi-square test of contingencies was used. The test was statistically significant (χ² (1, N = 79) = 6.61, p = .032), with male participants more likely to score above the clinical cut-off on the AQ-10. For male participants, 20 (36.4%) scored above the clinical cut-off, while for female participants, 7 (12.5%) scored above the clinical cut-off.

Group Differences: Impact of GMFCS

GMFCS level was not significantly associated with executive functioning. GMFCS level was significantly associated with inattention F(3, 70) = 3.75, p = .015, partial η2 = 0.138. Inattention scores were most elevated for children with a GMFCS level of II (M = 73.5, SD = 14.5). Means and standard deviations for each GMFCS level are displayed in Table 5.

After controlling for cognition, no statistically significant difference was found for different GMFCS levels on attention and behavioural domains, F(18, 181) = 1.51, p = .089, Wilks Λ = 0.673, partial η2 = 0.123. GMFCS level was not significantly associated with executive function domains after controlling for cognition, F(33, 171) = 0.768, p = .813, Wilks Λ = 0.666, partial η2 = 0.127.

Table 5 Means and Standard Deviations of Attention and Executive Function Domains by GMFCS Level (M = 50, SD = 10)
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Discussion

This study explores attention, behaviour, executive function and autism symptomatology in children with CP, as assessed by parent report for a representative population sample of school-aged children with CP. Across all domains, group mean scores were elevated for participants in this study when compared to the mean scores for the normative samples of same-aged children. Even when participant group mean scores were not in the clinically elevated range for certain measures, they were still above the population norm. This indicates that children diagnosed with CP are at increased risk of experiencing challenges with executive functioning, attention and impulsivity, behaviour, and symptoms of autism spectrum disorder, such as social communication difficulties. Additional analyses, controlling for cognitive ability as measured by the RCPM, indicated that the group means for the study sample remained elevated across all domains of attention and executive functioning when compared to the mean scores for the normative population samples of same-aged children.

Results on measures of autism symptomatology, inattention and hyperactivity/impulsivity suggest that risk of experiencing challenges in these areas increases further for male children diagnosed with CP. GMFCS level was not associated with reports of executive functioning, but was associated with inattention, with participants in the GMFCS II group reporting greatest impairment. However, after controlling for cognition, there was no longer a significant difference in attentional impairment between GMFCS groups.

Clinical Implications

These results highlight the need for screening for neurodevelopmental disorders in children with cerebral palsy, in line with recent clinical guidelines (National Guideline Alliance, 2017), as well as the importance of recognising significant executive dysfunction, inattention and autism symptomatology in children diagnosed with CP. It is essential to identify when a child diagnosed with CP is experiencing challenges with executive functioning, attention and impulsivity, and social communication. Not only can these factors impact aspects of everyday functioning, including education and participation (Bottcher et al., 2010), but also because such challenges can influence how a child might engage with all types of rehabilitation, such as physiotherapy, speech and occupational therapy (Craig et al., 2019). It is also important to keep in mind that monitoring should be ongoing. Skills related to EF continue to develop into early adulthood, and it is possible that subtle challenges may not emerge until later in a child’s developmental trajectory.

While choosing assessment measures for use with children with CP, there is a need to consider the heterogenous presentation of the population, in terms of motor function, communication, and cognitive ability. The parent-report measures used in this study are easily administered as part of a broader developmental or clinical assessment. Parent-report measures can provide insight into everyday functioning across attention, behaviour, executive function and social communication. Such measures could be included in general paediatric or psychological consultations in order to identify children with CP who are likely to benefit from full diagnostic assessment for attention deficit hyperactivity disorder, behavioural disorders, executive dysfunction and autism spectrum disorder.

It is also important to keep in mind that this study has found elevated scores across many domains at the group level for participants in this study, but on the individual level, various participants still scored within the typical range. This highlights the variability in outcome in a group as heterogenous as children with CP. While overall the group may be at greater risk for experiencing challenges in areas such as executive function, attention and behaviour, many individuals may not experience any such difficulties.

Limitations and Future Research

While the Conners-3 Short Form and the BRIEF are both diagnostic measures for ADHD and executive dysfunction, it is noted that best practice in diagnosis is for these measures to be given to multiple raters, for example both parents and teachers, and for results from these measures to be integrated with other sources of information, such as clinical interviews and observations. On their own, results from these measures cannot therefore be considered diagnostic. Similarly for ASD, the AQ-10 measure used in this assessment is a screening tool only, and diagnosis of ASD cannot be confirmed using this measure alone.

While parent-reported measures can provide insight into the impact of attentional and executive function challenges for children with CP, limitations with these measures have been reported for the population of children with CP. Although ratings scales are not directly impacted by a child’s motor or speech ability in the same way performance-based testing can be, differential motor or communication abilities may still render some items on parent-report measures invalid. Examples of this include items from the BRIEF such as – “Leaves playroom a mess,” or “Has trouble organizing activities with friends.” It is for this reason that data is not included for participants with GMFCS level V. It is possible that elevated scores for children with GMFCS level II are due to the greater utility and appropriateness of some items on the Conners-3 scales to children who are independently mobile. Future research into appropriate psychometric measures of attention, executive function and autism symptomatology for the full population of children with CP should be sensitive to motor and communication ability (Craig et al., 2019).

The gender ratio of this study is also noted as a limitation when considering generalisability. The percentage of males participating in this study (68.9%) is higher than the percentage of individuals born in the state who are male (56.9%). While the Conners-3 and BRIEF rating scales provide scores based on gender and age norms, the AQ-10 screener is scored according to clinical cut-off and does not account for gender. Research has indicated that ASD is more commonly diagnosed in males (Baron-Cohen et al., 2011). Therefore, a higher proportion of males in the current study may suggest a greater prevalence of ASD symptoms in the CP population than is otherwise warranted.

This study can also guide further research by highlighting potential areas for intervention, targeting executive function, attention and autism symptomatology for children diagnosed with CP. There are many potential areas of intervention including pharmacological treatments (Mechler et al., 2022), cognitive behavioural therapies (Lambez et al., 2020), computerised training, mindfulness, and physical exercise (Diamond & Lee, 2011; Lambez et al., 2020). Future studies following up children with CP as they enter adolescence and adulthood will also be valuable, to further understand the impact of challenges in these areas across the lifespan. This is particularly important as previous studies, including in the population of individuals with CP (Stadskleiv et al., 2016), indicate that executive functions continue to develop throughout adolescence and into early adulthood (Sørensen et al., 2016). As such, more subtle difficulties may become apparent later in a child’s developmental trajectory, as environmental demands and expectations increase. Key periods of transition include adolescence and the transition to secondary schooling, or early adulthood, with the end of formal schooling and entry into the workforce.

Conclusions

School-aged children with CP are at greater risk of symptomatology for other neurodevelopmental disorders, including attention deficit hyperactivity disorder, behavioural disorders, and autism spectrum disorder, with the risk even higher for male children. Parent-reported measures can be utilised as screening tools for comorbidities such as executive dysfunction, ADHD and ASD, and can identify areas for further clinical assessment and intervention.