Right Structural and Functional Reorganization in Four-Year-Old Children with Perinatal Arterial Ischemic Stroke Predict Language Production

Abstract

Brain imaging methods have contributed to shed light on the mechanisms of recovery after early brain insult. The assumption that the unaffected right hemisphere can take over language functions after left perinatal stroke is still under debate. Here, we report how patterns of brain structural and functional reorganization were associated with language outcomes in a group of four-year-old children with left perinatal arterial ischemic stroke (PAIS). Specifically, we gathered specific fine-grained developmental measures of receptive and productive aspects of language as well as standardized measures of cognitive development. We also collected structural neuroimaging data as well as functional activations during a passive listening story-telling fMRI task and a resting state session (rs-fMRI). Children with a left perinatal stroke showed larger lateralization indices of both structural and functional connectivity of the dorsal language pathway towards the right hemisphere that, in turn, were associated with better language outcomes. Importantly, the pattern of structural asymmetry was significantly more right-lateralized in children with a left perinatal brain insult than in a group of matched healthy controls. These results strongly suggest that early lesions of the left dorsal pathway and the associated perisylvian regions can induce the interhemispheric transfer of language functions to right homolog regions. This study provides combined evidence of structural and functional brain reorganization of language networks after early stroke with strong implications for neurobiological models of language development.

Signatures of brain plasticity supporting language recovery after perinatal arterial ischemic stroke

“…However, these results obtained in such a cross-sectional design did not provide information about the time course of the reorganization process. Nonetheless, they are in line with recent observations in a cohort of 4-year-old children with unilateral left PAIS in which a right-lateralized arcuate fasciculus as measured by the laterality index of the AF volume was associated with better expressive language based on utterance length (see Figure 3C; François et al, 2019). Taken together, these last studies suggest that the redundancy and bilateral organization of the language network can leave room for the functional and structural brain reorganization supporting the near-normal development of language functions.…”

“…First, there is evidence showing that early left hemisphere lesions can trigger the transfer of language functions in homologous brain regions of the right hemisphere (Tillema et al, 2008;Jacola et al, 2006;Ilves et al, 2014;Guzzetta et al, 2008;Lidzba et al, 2017a;François et al, 2016François et al, , 2019. For instance, Jacola and colleagues (2006) used fMRI with both a verb generation and a passive story listening task in three children aged 7, 9 and 10 years with unilateral left PAIS of the middle cerebral artery (MCA; see Table 1 for a summary of the neuroimaging studies on perinatal stroke).…”

“…Results have suggested a link between the microstructural properties of the arcuate fasciculus and language abilities (Salvan et al, 2017;Paldino et al, 2015). However, to our knowledge, only a few studies have gathered structural MRI together with behavioural and neuropsychological data in children with PAIS (François et al, 2016(François et al, , 2019Northam et al, 2018, see Figure 3 for a summary of the main results of the two last studies).…”

“…Taken together, these last studies suggest that the redundancy and bilateral organization of the language network can leave room for the functional and structural brain reorganization supporting the near-normal development of language functions. François et al, 2019). The lesion mask is shown in dark blue.…”

Pharmacotherapy of Traumatic Childhood Aphasia: Beneficial Effects of Donepezil Alone and Combined With Intensive Naming Therapy

“…For instance, studies of children with brain injury have shown that early damage to the AF may be succesfully compensated through recruitment of ipsilateral and contralateral brain areas and tracts, resulting in an average performance on multiple language tasks (Rauschecker et al, 2009;Asaridou et al, 2020), although some deficits may persist (Yeatman and Feldman, 2013). In this line, after early brain damage, functional and structural rightward lateralization of the dorsal pathway is associated with better language outcomes (Northam et al, 2018;Francois et al, 2019). Despite this evidence, spontaneous readjustment of the language system after brain lesion seems to be limited as evidenced by the frequent persistence of language deficits (Tavano et al, 2009;Turkstra et al, 2015;Francois et al, 2016).…”