Temporal processing impairment in children with attention-deficit-hyperactivity disorder
Highlights
► To investigate the temporal processing performance of Chinese children with ADHD by using time production, time reproduction paradigm and duration discrimination tasks. ► The findings showed that the probands with family history of ADHD performed significantly worse than those without family history in the time production tasks and the time reproduction task. ► The current findings suggest that provides further support for the existence of a generic temporal processing impairment in ADHD children and suggests that the time processing and ADHD share some common genetic factors.
Introduction
Temporal information processing refers to the analysis of stimulus time patterns. Central systems that decode temporal information and record time series (Mauk & Buonomano, 2004) allow perception and organization of sequences of events and actions and facilitate anticipation or prediction of when future events will occur (Toplak, Dockstader, & Tannock, 2006). A number of theoretical models of how the brain organizes and stores events for the future use have been suggested, and the ‘internal clock’ model has been widely accepted (Matell and Meck, 2000, Matell and Meck, 2004). Within this model, Zakay has emphasized the role of attention in temporal processing and proposed an “Attentional-Gate Model” (Zakay, 2000).
Attention deficit hyperactivity disorder (ADHD) is a cognitive developmental disorder characterized by levels of inattention, hyperactivity, and impulsivity that are age-inappropriate. Growing evidence links ADHD to problems in several aspects of temporal information processing, including duration discrimination, duration reproduction, and finger tapping and it has been suggested that deficits in temporal information processing contribute to poor cognitive and behavioral outcomes (Toplak et al., 2006). However, temporal information processing is a multidimensional construct that has spurred the development of a wide variety of methods designed to quantify its component abilities. Consequently it is difficult to integrate findings across studies of temporal information processing in the field of ADHD.
Two models offer an explanation of how temporal processing might be impaired in ADHD. The most common, behavioral inhibition, argues that poor inhibitory control and interference affect working memory, which subsequently affects temporal processing (Barkley, 1997). In contrast, the delay aversion concept, considers the primary deficit in ADHD is a preference for immediate reward or an aversion to delay (Sonuga-Barke, 2003) rather than a deficit in their working memory. Inter-connected circuitry through frontal, striatal, parietal, temporal and cerebellar regions that are involved in time perception, inhibitory control and reward-related behavior have consistently been implicated in the pathophysiology of ADHD (Carmona et al., 2011, Cubillo et al., 2011a, Cubillo et al., 2011b, Posner et al., 2011, Scheres et al., 2010, Sonuga-Barke et al., 2010), and empirical evidence has shown that children with ADHD have deficits in time production (van Meel, Oosterlaan, Heslenfeld, & Sergeant, 2005), time reproduction (Bauermeister et al., 2005, Carelli et al., 2008, Gonzalez-Garrido et al., 2008, Kerns et al., 2001, Meaux and Chelonis, 2003, Rommelse et al., 2007, Smith et al., 2002, Sonuga-Barke et al., 1998, Toplak et al., 2003), and motor timing tasks (Rubia et al., 2003, Rubia et al., 1999). However, there is no consensus on the performance of time discrimination tasks in ADHD (Radonovich and Mostofsky, 2004, Toplak et al., 2005, Yang et al., 2007) and many previous studies of temporal processing in ADHD have been limited by small sample sizes and did not include subtypes of ADHD, e.g., ADHD with inattention, and ADHD with combined hyperactivity and inattention (Richard, Balentine, & Lynam, 2001).
Time discrimination in ADHD might depend upon the length of time interval examined. Some have suggested that the processing of short intervals (less than 1 s) may rely on an internal timing mechanism or cerebellar process, whereas longer intervals (1 s or greater) may access working memory processes (Ivry, 1996, Mangels et al., 1998). The attentional-gate model predicts that when intervals exceed the range that is relevant for typical sensory events, greater demands is placed on other cognitive functions such as sustained attention and working memory (Mangels, Ivry, & Rapp, 2001). In a previous study (Yang et al., 2007), children with ADHD were asked to discriminate between 2 sets of time interval: one was less than 1 s, the other longer than 1 s. We found that children with ADHD had significantly higher discrimination thresholds than healthy controls, and there was an interaction effect between group and duration. Children with ADHD were also less accurate in discriminating the duration of stimuli. Working memory was associated with the discrimination threshold at a duration of 800 ms after controlling for FIQ in ADHD children.
Discrimination of brief intervals has been represented as a candidate endophenotype for ADHD (Himpel et al., 2009). Since twin and family studies indicate that attention problems have a major genetic component explaining up to 80% of the total variance (van’t Ent et al., 2009), confirming a temporal processing endophenotype for ADHD could offer a useful translational tool for further investigation of genetic factors. Therefore we planned a study to replicate and extend our previous findings and investigate whether subtype of ADHD and family history differentially impacts upon temporal processing in ADHD.
We also wished to examine multiple aspects of temporal processing capacity in children with ADHD. For example, the difficulty children with ADHD have in time reproduction task might be explained by an inhibition difficulty rather than a ‘pure’ temporal processing anomaly (Sonuga-Barke, Saxton, & Hall, 1998). Therefore, in the present study, we employed two time reproduction tasks to rule out the impact of inhibition deficit. One had two conditions: the signaled condition (SC) to control for response inhibition and the unsignaled condition (USC) to reproduce time. Sonuga-Barke et al. have argued that if the subject can respond correctly in the SC while performing poorly in the USC, any deficit could not be explained by inhibition impairment and was due to a temporal processing impairment (Sonuga-Barke et al., 1998). However the latter result has been questioned because the visual structure of the signals used in SC and USC were different (Smith et al., 2002, Sonuga-Barke et al., 1998). In the current study we adapted this paradigm to minimize any visual structural difference in the task conditions.
Another possible confound in the study of time perception in ADHD is the impact of motor demands. The organization of motor output is heavily dependent on the representation of time in the brain, and motor difficulties also characterize individuals with ADHD (Carte et al., 1996, Riordan et al., 1999). Moreover, time perception and motor coordination share the same underlying neural system, which is predominantly a right hemispheric fronto-striato-cerebellar network (Smith et al., 2003). Unlike time production and reproduction tasks, the duration discrimination tasks minimize the motor demands of timing performance (Carte et al., 1996, Riordan et al., 1999) and have no speed requirement, therefore time discrimination was also examined in the present study.
Based on previous findings, we hypothesized that children with ADHD would have significant differences in multiple tasks of temporal processing compared to typically developing control children. We also predicted that children with ADHD (probands), with a family history of ADHD, would perform more poorly in temporal processing tasks than those without a family history.
Section snippets
Participants
The selection and assessment of the participants has been described in detail elsewhere (Yang et al., 2007). In brief, the children with ADHD were recruited from consecutive referrals to three child behavioral clinics that serve large urban populations in Guangdong Province, China. Handedness was assessed by means of the Annett Hand Preference Questionnaire (Annett, 1976). Inclusion in the study required an ICD-10 diagnosis of ADHD based on clinical semi-structured parent and child interviews
Temporal processing functions
Repeated measures MANOVA was used to analyze performances in the time production task, time reproduction task and the time discrimination task, with the target duration as a repeated measurement factor, group as inter-subject factor, and FIQ as covariate (see Table 2). The Huynh–Feldt (HF-F) values in F-test were used to indicate statistical significance because the results of Mauchly Sphericity test were significant.
Discussion
ADHD is characterized by levels of inattention, hyperactivity, and impulsivity that are age-inappropriate. The results of the current study provide evidence for specific deficits in temporal processing in ADHD.
Declaration of interest
None.
Acknowledgements
This study was supported partially by the Project-Oriented Hundred Talents Programme (O7CX031003) of the Institute of Psychology, Chinese Academy of Sciences, the Knowledge Innovation Project of the Chinese Academy of Sciences (KSCX2-EW-J-8), the National Science Fund China Young Investigator Award (81088001), and the Research Initiation Grant from the Sun Yat-Sen University (16000-3253182) to Raymond Chan. This study was partially supported by the Young Investigator Scientific Fund of
References (55)
- et al.
Fronto-striatal underactivation during interference inhibition and attention allocation in grown up children with attention deficit/hyperactivity disorder and persistent symptoms
Psychiatry Research
(2011) - et al.
ADHD subtypes do they differ in their executive functioning profile?
Archives of Clinical Neuropsychology
(2005) The representation of temporal information in perception and motor control
Current Opinion in Neurobiology
(1996)- et al.
Dissociable contributions of the prefrontal and neocerebellar cortex to time perception
Brain Research, Cognitive Brain Research
(1998) - et al.
Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes
Cognitive Brain Research
(2004) - et al.
Time perception differences in children with and without ADHD
Journal of Pediatric Health Care
(2003) - et al.
Neuropsychological executive functions and DSM-IV ADHD subtypes
Journal of the American Academy of Child and Adolescent Psychiatry
(2002) - et al.
Differences in academic and executive function domains among children with ADHD predominantly inattentive and combined types
Archives of Clinical Neuropsychology
(2006) - et al.
Neuropsychological correlates of methylphenidate treatment in adult ADHD with and without depression
Archives of Clinical Neuropsychology
(1999) - et al.
Time reproduction in children with ADHD and their nonaffected siblings
Journal of the American Academy of Child and Adolescent Psychiatry
(2007)
Temporal reward discounting in attention-deficit/hyperactivity disorder: the contribution of symptom domains, reward magnitude, and session length
Biological Psychiatry
Beyond the dual pathway model: evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder
Journal of the American Academy of Child and Adolescent Psychiatry
The role of interval underestimation in hyperactive children's failure to suppress responses over time
Behavioral Brain Research
The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics
Neuroscience and Biobehavioral Reviews
Temporal information processing in ADHD: findings to date and new methods
Journal of Neuroscience Methods
Neuroimaging of response interference in twins concordant or discordant for inattention and hyperactivity symptoms
Neuroscience
Motivational effects on motor timing in attention-deficit/hyperactivity disorder
Journal of the American Academy of Child and Adolescent Psychiatry
Time perception deficit in children with ADHD
Brain Research
Gating or switching? Gating is a better model of prospective timing (a response to ‘switching or gating?’ by Lejeune) (Reprinted from Behavioural Processes, 50, 1–17, 1998)
Behavioural Processes
Attention deficit/hyperactivity disorder(ADHD): complex phenotype, simple genotype?
Genetics in Medicine
The classification of child psychopathology: a review and analysis of empirical efforts
Psychological Bulletin
A coordination of hand preference and skill replicated
British Journal of Psychology
Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD
Psychological Bulletin
Time estimation and performance on reproduction tasks in subtypes of children with attention deficit hyperactivity disorder
Journal of Clinical Child and Adolescent Psychology
A comparison of North American versus non-North American ADHD study populations
European Child and Adolescent Psychiatry
Sense of time and executive functioning in children and adults
Child Neuropsychology
Response inhibition and reward anticipation in medication-naive adults with attention-deficit/hyperactivity disorder: a within-subject case-control neuroimaging study
Human Brain Mapping
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2013, NeuropsychologiaCitation Excerpt :Thus, twenty one studies explored group differences in duration reproduction between participants with ADHD and healthy controls (Barkley et al., 1997, 2001b; Barkley, Murphy, & Bush, 2001a; Bauermeister et al., 2005; González-Garrido et al., 2008; Gooch et al., 2011; Hurks and Hendriksen, 2010; Huang et al., 2012; Hwang, Gau, Hsu, & Wu, 2010; Kerns, McInerney, & Wilde, 2001; Marx et al., 2010; McInerney & Kerns, 2003; Meaux & Chelonis, 2003; Mullins, Bellgrove, Gill, & Robertson, 2005; Plummer & Humphrey, 2009; Rommelse, Oosterlaan, Buitelaar, Faraone, & Sergeant, 2007; Smith et al., 2002; Toplak et al., 2003 (two experiments); Valko et al., 2010; West et al., 2000). The most consistent finding is that of decreased reproduction accuracy (González-Garrido et al., 2008; Smith et al., 2002; Toplak et al., 2003), higher absolute discrepancy scores (Barkley et al., 1997, 2001a, 2001b; Bauermeister et al., 2005; Gooch et al., 2011; Huang et al., 2012; Hwang et al., 2010; Kerns et al., 2001; Marx et al., 2010; McInerney & Kerns, 2003; Meaux & Chelonis, 2003; Mullins et al., 2005; Plummer & Humphrey, 2009; Rommelse et al., 2007; Valko et al., 2010; West et al., 2000), and increased SDintra of reproduced intervals in ADHD patients relative to controls (Mullins et al., 2005; Toplak et al., 2003; Valko et al., 2010) (see Table 2). Abnormal duration reproduction in ADHD was observed in all age groups: in children (Barkley et al., 1997; Bauermeister et al., 2005; González-Garrido et al., 2008; Gooch et al., 2011; Huang et al., 2012; Hurks & Hendriksen, 2010; Kerns et al., 2001; McInerney & Kerns, 2003; Meaux & Chelonis, 2003; Mullins et al., 2005; Plummer & Humphrey, 2009; Rommelse et al., 2007; Smith et al., 2002; Toplak et al., 2003; Valko et al., 2010; West et al., 2000), adolescents (Barkley et al., 2001b; Hwang et al., 2010; Marx et al., 2010; Toplak et al., 2003) and adults with ADHD (Barkley et al., 2001a; Marx et al., 2010).
Time perception in children: A neurodevelopmental approach
2013, Neuropsychologia
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These authors contributed equally.