Evaluation of a neurotherapy program for a child with ADHD with Benign Partial Epilepsy with Rolandic Spikes (BPERS) using event-related potentials

Background

Rolandic epilepsy (RE) is the most common epilepsy syndrome affecting children [1]. It is a developmental epilepsy with a complex genetic inheritance that has yet to be elucidated [2]. Centrotemporal spikes (CTS) are the electroencephalographic hallmark [1].

RE is also known as benign rolandic epilepsy of childhood (BREC) or benign epilepsy with centro-temporal spikes (BECTS) [3]. ‘Rolandic’ means that the seizures begin in the part of the brain called the Rolandic area. The seizures are classified as a partial seizure because only this one part of the brain is involved [4–6].

The syndrome is called ‘benign’ because it has a good outcome: nearly all children with RE will outgrow it during puberty. It affects almost one in five of all children who have epilepsy. which makes it is one of the most common types of epilepsy in children. It affects boys and girls equally. RE usually begins between the ages of 3 and 10 years, and often stops around puberty (age 14–18) [6,7].

Some children who have this type of epilepsy are usually well otherwise and do not have learning difficulties, although some may have specific difficulties with reading and language or with drawing and visuo-spatial skills [1,4,8,9], and some have associated neuropsychiatric deficits resembling the symptoms of attention deficit-hyperactivity disorder (ADHD), the most common neurobehavioral disorder of childhood [7,9].

It was gradually realized that there was a close relationship between benign partial epilepsy with Rolandic Spikes (BPERS) and acquired epileptic aphasia (Landau-Kleffner syndrome), which was the first example of a mainly “cognitive” epilepsy in children [9]. Prolonged reversible oral-motor deficits were subsequently recognized during the active epilepsy phase in some children with an otherwise typical syndrome and good final prognosis. These cases showed that this epilepsy syndrome could cause prolonged “epileptic” deficits. Several neuropsychological studies confirmed the clinical experience that children with BPERS had normal intelligence but that a certain percentage of them showed variable attention or selective deficits (linguistics, visuospatial etc.), as compared to normal controls [1,8,9].

Recent studies on the frequent temporary cognitive-behavioral disorders encountered in BPERS have placed emphasis on their probable direct epileptic origin [9]. This was thought to possibly explain some of the learning and school problems that many of these children experienced in the active phase of the syndrome. Rare longitudinal correlative EEG-neuropsychological studies have recently shown that acquired temporary cognitive-behavioral problems correlate with epileptic activity (EEG) in some children [6,10,11]. It is now an open question whether this epilepsy can cause a specific developmental learning disability, or more general cognitive disability, if the onset is severe, early, and affects brain areas other than the strictly “rolandic” [10].

To this end, event-related potentials (ERPs) were measured during a visual 1-backmatching task. EEG spectra and ERPs in a patient with Rolandic interictal spikes were compared with the normative data (HBIdatabase) in order to estimate the main neurophysiological deficits found in this patient.

The deviations from the normality are discussed in term of well-known pathophysiological patterns in the ADHD population, such as increased in the theta-beta ratio [5], decrease of the P3b component [6–8] and decrease of the P3 NOGO potential [9,10]. A quantitative analysis technique to analyze the ERP data, without any “a priori” decisions on “peak” presence, amplitudes or latencies, is used. The frequency of rolandic spikes in children with ADHD is significantly higher than that expected from epidemiologic studies. Also, ERPs are of significantly higher amplitude in the epilepsy group compared to the control group over frontal and central regions within the time window between 250 and 425 ms post-stimulus, which coincides with the time window of target-nontarget stimulus discrimination [1,3,4].

The question arises how ADHD symptoms are related to rolandic spikes in this ADHD subgroup and how these symptoms can be treated by neurotherapy. What follows is a case study, in which we address this question.

The aim of this study was to find out:

Case Report

Behavioral data

BEHAVIORAL DATA:

The results of a comparison of the patient’s behavioral parameters during the GO/NOGO task are presented in Table 2. The number of omission errors decreased by more than 50% after treatment, so that no deviation in behavior from norms was observed after treatment.

SPECTRA: Deviations from normality in the EEG spectra computed for 20 minutes of the GO/NOGO task before treatment are presented in Figure 8 left. As one can see the EEG pattern is characterized by excessive slow (around 6 Hz) activity over frontal-temporal areas. Quite large and statistically significant changes occurred after treatment. The excessive slow activity decreased after treatment (Figure 8, right).

EVENT RELATED POTENTIALS: The results of ERP changes are presented in Figure 9. One can see dramatic changes of the NOGO ERPs with increase of the NOGO potential over the Cz electrode and decrease over the left temporal areas.

Discussion

WHY DID WE NOT ACHIEVE FULL RECOVERY?:

BPERS is a model for the study of the cognitive manifestations of focal epileptic discharges in a developing brain, although the prolonged fluctuating and cognitive manifestations and their dynamics of onset and recovery cannot be explained in terms of simple ictal-postictal symptoms which suggest that several different mechanisms are probably involved.

THEREFORE, HOW TO INTERPRET OUR RESULTS?:

Microgenetic theory [30] makes it possible to interpret the results we have achieved. This theory differs from other theories of brain function in that it emphasizes:

In particular, a fuller understanding of the essence of ADHD brings us closer to grasping the process of symptom formation.

In Figure 10, the afferent pathways bring impulses received from the sense organs to the brainstem, which constitutes the oldest and most primitive part of the brain. The brainstem reacts with a general activation of the organism, which is transmitted upwards (A), to the limbic system and cerebellum. From these somewhat younger structures the activation signal becomes more complex (B), so that in the cortex it spreads to highly specialized areas. Signals from the cortex then travel by pyramidal pathways back down to the brainstem, and from there by efferent pathways to effectors in the musculoskeletal system.

Understanding this somewhat simplified diagram of activation makes it easier to interpret the mosaic of diverse disturbances that occur in children with AD/HD, associated with disturbances that are both structural (involving different areas and different levels of the brain) and functional (resulting from changes on the level of neurotransmission), as well as the resolution of these disturbances in the course of rehabilitation.

The process of symptom formation responsible for the heterogeneity and changeability of behavioral disturbances in ADHD children is explained by Figure 11, which illustrates the bidirectional transition from emotion to mentation and action. The state of arousal in the mind, which in a healthy brain can be reinforced or inhibited by the executive functions, cannot be controlled in the brains of ADHD children. Thus the behavior which these children exhibit can be diverse, variable, and capricious, depending on a whole range of factors both structural and functional in nature.