The time window for successful right-hemispheric language reorganization in children

https://doi.org/10.1016/j.ejpn.2017.06.001Get rights and content

Highlights

  • Left-hemispheric stroke until age five years had favorable language outcome.

  • Until age two years, right-hemispheric language reorganization was functionally successful.

  • After age five years, good recovery with left-hemispheric (peri-lesional) reorganization.

Abstract

Aim

To identify, in a retrospective, observational study, the time window during which successful right-hemispheric language reorganization is possible after left-hemispheric brain damage.

Method

25 patients (10 females; age 6–41 years; ≥12 months after insult; age at insult 0;3–15;11 years) with acute, language-relevant left-hemispheric insults acquired during childhood and adolescence completed questionnaires for self-assessment of language problems. 12 patients of those reporting no (n = 8) or only moderate (n = 4) language problems participated in language fMRI.

Results

Language outcome of lesions occurring before 5 years of age (n = 7) was always favorable, and language was right-lateralized (2 patients: age at lesion < 2 years) or bilateral (3 patients: age at lesion 2–5 years). Following lesions occurring after 5 years of age, language outcome was often unfavorable (11/18 patients: moderate or severe problems), and of the 7 patients without problems, none showed right-hemispheric reorganization (fMRI available in 4).

Interpretation

The combination of normal language outcome and right-hemispheric language reorganization after a left-hemispheric lesion sustained after the neonatal period is extremely rare. Functionally sufficient right-hemispheric language was documented in only two patients with lesions acquired before two years of age.

Introduction

The superior compensatory potential of the developing right hemisphere for language is one of the most prominent examples of early brain plasticity.1 Extensive lesions to the left hemisphere, which result in severe and persisting language problems when acquired in adulthood, can often be compensated when the lesions occur perinatally by “shifting” language to the undamaged right hemisphere.1 The relation of reorganization pattern and language outcome in children with perinatal stroke is not yet clearly determined. Atypical language lateralization (i.e., right-hemispheric or bilateral) was associated with better language performance in one study,2 but with worse performance in another.3 Generally, perinatally acquired left-hemispheric lesions may cause delayed language acquisition,4 but by school age, most children perform normally under naturalistic conditions.5, 6 Only when confronted with linguistically complex tasks do they show deficits, e.g., in grammar processing7 and discourse.8 Developmental functional brain imaging studies have demonstrated an initially strong right-hemispheric involvement in language development9 with increasing left-lateralization during childhood and even adolescence.10, 11, 12 Based on these data, one may assume that during this dynamic phase, right-hemispheric language reorganization after acute left-hemispheric lesions might be more successful than in adulthood. The time period when the right hemisphere loses the potential to successfully take over language function, however, has not been determined yet. After acute lesions occurring in the course of childhood and adolescence, right-hemispheric language dominance seems to be rare.13 In those with documented aphasia, right-hemispheric language representation in the chronic phase is more frequent, however, mostly in those children still performing poorly on language tasks.14 It seems, thus, that right-hemispheric language reorganization associated with satisfactory language outcome might be a phenomenon observed in the very immature brain only. The aim of our study was to define the age until which the right hemisphere is indeed able to satisfactorily take over language function after an acute left-hemispheric insult.

The current lack of information on this plastic time-window becomes critical when it comes to the treatment of children with a potentially progressive epileptic disease of the left hemisphere (e.g., Rasmussen’s encephalitis). While the epilepsy may respond to pharmacological intervention for a long time, surgical intervention might later become necessary. And how can we know if the “plastic window” enabling interhemispheric language reorganization will, then, still be open, protecting the child from persistent aphasia? With better data on the time-course of neural plasticity, it would be easier to decide how long to “wait and see”.

Many previous publications on successful right-hemispheric language reorganization after lesions acquired during childhood report on patients with therapy-refractory epilepsies who underwent fMRI or Wada testing during their pre-surgical work-up, or who received left hemispherectomies.1, 15, 16 In most of these patients, however, the age at onset of the underlying disorder (e.g., Rasmussen's encephalitis) and, therefore, the age at onset of the reorganizational process, cannot precisely be determined. For the current study, we recruited a highly selective sample of patients with acute left-hemispheric insults, a history of aphasia or, in preverbal children, MRI evidence for lesions in language relevant areas, and without any evidence for pre-existing brain pathologies, so that the age at insult could safely be taken for the onset of reorganization. We excluded patients with pre-, peri- or neonatal lesion onset (although much more easily available) since for these, satisfactory language outcome of right-hemispheric reorganization has already been demonstrated.5, 6

Section snippets

Participants

For this retrospective study, the clinical databases of two large neuropediatric centers (Schön Klinik Vogtareuth and University Children’s Hospital Tübingen) were searched for patients with left-hemispheric brain lesions, acquired ≥ 12 months before the study, at an age between 4 weeks and 18 years, without evidence for pre-existing brain anomalies or epilepsy, and aphasia >4 weeks post insult as documented by a speech/language pathologist, or, if younger than 24 months at time of insult, MRI

Results

Out of 36 patients contacted, 25 returned the questionnaire (Table 1), 11 did not reply. Follow-up latency was 2–32 years after the pathological event. Twenty-two patients reported “no” or only “moderate” persisting language problems, and were invited for fMRI. Seven of these patients could not be scanned due to MR contraindications (anxiety, metal implants, dental braces), 3 did not reply to the second invitation. In the remaining 12 patients, fMRI scans could successfully be performed.

Two age

Discussion

How long is the right hemisphere able to successfully “take over” language in children? A satisfying answer to this question would have relevant implications not only to our understanding of the developing brain’s plasticity. It could also aid in the decision process regarding neurosurgery for young children with catastrophic epilepsy.

Our data indicate that the compensatory potential of the right hemisphere might already be limited at the age of 5 years: Incomplete recovery from aphasia started

Sources of funding

University Tübingen's Medical Faculty (AKF 308-0-0). The funding source had no influence on study design, data analysis, or the decision to report the results.

Conflict of interest

Dr. Lidzba and Dr. Küpper: none.

Dr. Kluger: honoraria from serving on the scientific advisory board of Eisai GmbH.

Dr. Staudt: travel compensation for speaking at educational meetings from Desitin.

References (28)

  • W.S. Helton et al.

    Cerebral lateralization of vigilance: a function of task difficulty

    Neuropsychologia

    (2010)
  • A.M. Chilosi et al.

    Acquired focal brain lesions in childhood: effects on development and reorganization of language

    Brain Lang

    (2008)
  • T. Rasmussen et al.

    The role of early left-brain injury in determining lateralization of cerebral speech functions

    Ann N Y Acad Sci

    (1977)
  • P. Ilves et al.

    Different plasticity patterns of language function in children with perinatal and childhood stroke

    J Child Neurol

    (2014)
  • Cited by (0)

    View full text