Evidence for modulation of planning and working memory capacities by transcranial direct current stimulation in a sample of adults with attention deficit hyperactivity disorder

Highlights

• The London Tower Test performance was enhanced after active tDCS in adults with ADHD.

• The backward digit span improved after active tDCS.

• No improvements were observed in the Continuous Performance Test and Stroop Test after active tDCS.

Abstract

Background and Objective

Attention deficit hyperactivity disorder (ADHD) is a common neurodevelopmental disorder that affects up to 2.8% of the adult population. Albeit pharmacological and behavioral therapies alleviate some core symptoms of ADHD, they do not avail cognitive dysfunction adequately. Executive dysfunction has been considered to have a principal role in ADHD and has previously been linked to activity alterations in the prefrontal cortex. Transcranial Direct Current Stimulation (tDCS) is a noninvasive brain stimulation technique that may modulate prefrontal cortex activity and induce neuroplasticity, with preliminary results in ADHD. The aim of the present study is to assess the effect of repeated tDCS on measures of executive functions in adults with ADHD.

Method

In this randomized double-blind sham-controlled study, 22 adults with ADHD were allocated into two groups and were administered five consecutive sessions of 2 mA active/sham tDCS over the dorsolateral prefrontal cortex (right anodal/left cathodal). A neuropsychological test battery was administered before the first session and immediately after the last session.

Results

The maximum number of digits and the total number of correct trials in the Digit Span Backward test increased in the active group (p = 0.017). The total move score in the Tower of London test decreased (p = 0.033), suggesting better planning ability. However, no significant differences were observed on Stroop Test and Trail Making Test after tDCS.

Discussion

The present study corroborates the modulating effects of tDCS on planning and working memory in a small group of adults with ADHD. Our results highlighted that cognitive functions are modulable using tDCS in adults with ADHD.

Introduction

Attention Deficit Hyperactivity Disorder (ADHD) is a neurodevelopmental disorder that appears in early childhood and may continue into adulthood [1]. The early definitions, which maintain validity, proposed that the neurocognitive profile of ADHD presents with impulsivity, hyperactivity and inattention [2]. Hyperactivity, distractibility and impulsivity symptoms that are seen in human prefrontal cortex (PFC) lesions may share similar behavioral features with cognitive dysfunction in ADHD; possibly stemming from the diminished functional connectivity between the PFC with the subcortical structures, i.e., basal ganglia and the thalamus [3]. Accordingly, a meta-analysis of 83 studies comparing the cognitive abilities of patients with ADHD and control groups revealed poor performance in executive functions as a common finding [4]. Among these executive functions, commonly reported cognitive deficits in adults with ADHD include attention, response inhibition, vigilance and working memory [5].

The cognitive deficits in ADHD have also been conceptualized to include deficits in the reward system, manifesting in the deficits of response delay [6]. The inability to delay impulsive responses causes immature reactions that are insufficient to reach long-term goals. Thus, patients with ADHD are reported to perform poorly on problem-solving tasks, particularly prominent in tower tests, i.e., the Tower of London (ToL) and the Hanoi Towers [7].

Digit span is a commonly used test to evaluate numerical recall and attentional capacity as well as working memory. Previous studies report that the adult patients with ADHD almost have similar forward digit span while performing worse than controls on the backward digit span [8]. Even though there is cognitive heterogeneity in adults with ADHD, some reports indicated a deficit with almost medium effect size (Cohen’s d = 0.37) in digit span backwards test [9]. Additionally, studies frequently focus on patients' attentional functions using tasks that require sustained attention. Among those, the Continuous Performance Test [10] is the most frequently used computerized test which enables distinguishing the cognitive features between control groups and ADHD patients in behavioral measures such as the number of errors (omission and commission) and reaction times [11]. Besides the patterns of omission and commission errors, patients with ADHD are found to have more reaction time variability than healthy controls [12]. One of the primary difficulties in comparing results across studies using a CPT paradigm is the variation through the versions. The AX-CPT version requires to direct attention, discriminate stimuli with preceding condition, and inhibit inappropriate response tendencies [13], [14]. Considering that impulsivity might be observed in ADHD, the task of monitoring the preceding stimulus may provide a stronger challenge for cognitive control by engaging inhibitory networks.

The present study focused on the stimulation of the right dorsolateral PFC (dlPFC) as disrupted attentional processes in ADHD have been consistently related with hypoactivation of the right dlPFC, right inferior parietal cortex, and subcortical connections of these areas [3]. Functional magnetic resonance imaging (fMRI) studies have shown an increase in blood oxygenation level-dependent (BOLD) response in the dlPFC during the tasks involving planning and decision-making skills. It has been well documented that the dlPFC is mostly utilized when external information is required to be kept online, re-organized, and used for goal directed behaviors [15]. Recently, a large meta-analysis of fMRI studies has also reported reduced activity at right hemispheric dorsal attention network, mainly encompassing the right dlPFC and the right inferior parietal cortex during selective, divided and sustained attention in individuals with ADHD [16]. Consequently, the right dlPFC and right inferior frontal cortex may be candidate regions for neurotherapeutics such as neuromodulation in individuals with ADHD.

Neuromodulation is the process of providing modifications on neural activity engaging the electrical or the chemical stimulating methods. This modulation provides the possibility of regulating the central, peripheral or autonomic nervous system for therapeutic purposes either inhibiting or exhibiting the targeted neural activity [17]. Repetitive Transcranial Magnetic Stimulation (rTMS) and transcranial Direct Current Stimulation (tDCS) are the neuromodulation-based treatment methods. The remediation effect of tDCS has been examined in many neuropsychiatric conditions such as Alzheimer's Disease [18], schizophrenia [19] and obsessive–compulsive disorder [20].

Although ADHD has been another interest of tDCS studies, according to our knowledge, the number of double-blind randomized sham-controlled studies in adult individuals is limited. While three of them have reported the result of a single session application [21], [22], [23], another study had reported a series of three tDCS sessions per week [24]. Cachoeira et al. contributed to the literature by evaluating the results of five consecutive days of application in terms of behavioral symptoms of 17 ADHD patients, but the neuropsychological evaluation was not involved [25].

Regarding the enhancing results of tDCS on cognitive functions in individuals with ADHD children and adults, we hypothesized that five consecutive sessions of tDCS would enhance cognitive functions in individuals with ADHD. Thus, we aim to assess the effect of five sessions of right anodal/left cathodal tDCS in individuals with ADHD with a selected battery of neuropsychological tests.