Limitations on the developing preterm brain: Impact of periventricular white matter lesions on brain connectivity and cognition

Department of Paediatric Neurology and Developmental Medicine, Children's Hospital, Medical School, Eberhard Karls University of Tübingen, Hoppe-Seyler-Strasse 1, 72076 Tübingen, Germany. .
Brain (Impact Factor: 9.2). 04/2013; 136(Pt 4):998-1011. DOI: 10.1093/brain/aws334
Source: PubMed


Brain lesions to the white matter in peritrigonal regions, periventricular leukomalacia, in children who were born prematurely represent an important model for studying limitations on brain development. The lesional pattern is of early origin and bilateral, that constrains the compensatory potential of the brain. We suggest that (i) topography and severity of periventricular lesions may have a long-term predictive value for cognitive and social capabilities in preterm birth survivors; and (ii) periventricular lesions may impact cognitive and social functions by affecting brain connectivity, and thereby, the dissociable neural networks underpinning these functions. A further pathway to explore is the relationship between cerebral palsy and cognitive outcome. Restrictions caused by motor disability may affect active exploration of surrounding and social participation that may in turn differentially impinge on cognitive development and social cognition. As an outline for future research, we underscore sex differences, as the sex of a preterm newborn may shape the mechanisms by which the developing brain is affected.

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Available from: Marina Pavlova, Jan 12, 2016
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    • "Schizophrenia occurs 1.4 times more frequently in males than females, and the onset of disease is earlier in men (Picchioni and Murray 2007). Males are at a 14–20% higher risk for premature birth and of its complications in the brain development and cognition (Pavlova and Krägeloh-Mann 2013). Males are more often affected by attention deficit hyperactivity disorder, ADHD (Bloom et al. 2012). "
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    • "Due to its rapidly developing and complex characteristics, the preterm brain is vulnerable to exogenous and endogenous insults in the third trimester of gestation (Volpe, 2009), during which the volume of the whole brain more than doubles and the volume of cortical grey matter (GM) increases approximately four-fold (Huppi et al., 1998). Therefore , attention has increasingly focused on the quality of life of survivors, who are at greater risk of brain damage and consequent neurological disorders, neuropsychological, and behavioural impairments in childhood and later in life (Ball et al., 2013; Beauchamp et al., 2008; Bjuland et al., 2013; Johnson and Marlow, 2011; Ment et al., 2009; Pavlova and Krageloh-Mann, 2013; Taylor et al., 2011). "
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    ABSTRACT: Alterations in cortical development and impaired neurodevelopmental outcomes have been described following very preterm (VPT) birth in childhood and adolescence, but only a few studies to date have investigated grey matter (GM) and white matter (WM) maturation in VPT samples in early adult life. Using voxel-based morphometry (VBM) we studied regional GM and WM volumes in 68 VPT-born individuals (mean gestational age 30 weeks) and 43 term-born controls aged 19–20 years, and their association with cognitive outcomes (Hayling Sentence Completion Test, Controlled Oral Word Association Test, Visual Reproduction test of the Wechsler Memory Scale-Revised) and gestational age. Structural MRI data were obtained with a 1.5 Tesla system and analysed using the VBM8 toolbox in SPM8 with a customized study-specific template. Similarly to results obtained at adolescent assessment, VPT young adults compared to controls demonstrated reduced GM volume in temporal, frontal, insular and occipital areas, thalamus, caudate nucleus and putamen. Increases in GM volume were noted in medial/anterior frontal gyrus. Smaller subcortical WM volume in the VPT group was observed in temporal, parietal and frontal regions, and in a cluster centred on posterior corpus callosum/thalamus/fornix. Larger subcortical WM volume was found predominantly in posterior brain regions, in areas beneath the parahippocampal and occipital gyri and in cerebellum. Gestational age was associated with GM and WM volumes in areas where VPT individuals demonstrated GM and WM volumetric alterations, especially in temporal, parietal and occipital regions. VPT participants scored lower than controls on measures of IQ, executive function and non-verbal memory. When investigating GM and WM alterations and cognitive outcome scores, subcortical WM volume in an area beneath the left inferior frontal gyrus accounted for 14% of the variance of full-scale IQ (F = 12.9, p < 0.0001). WM volume in posterior corpus callosum/thalamus/fornix and GM volume in temporal gyri bilaterally, accounted for 21% of the variance of executive function (F = 9.9, p < 0.0001) and WM in the posterior corpus callosum/thalamus/fornix alone accounted for 17% of the variance of total non-verbal memory scores (F = 9.9, p < 0.0001). These results reveal that VPT birth continues to be associated with altered structural brain anatomy in early adult life, although it remains to be ascertained whether these changes reflect neurodevelopmental impairments or long lasting structural alterations due to prematurity. GM and WM alterations correlate with length of gestation and mediate cognitive outcome.
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    • "For Down syndrome, the reported sex ratio is 1.28 [51], and for fragile X syndrome, the ratio is 2 [52]. Males are at a 14–20% higher risk for premature birth [53] and of its complications in the brain development and cognition [54]. On the other hand, depression is approximately twice as common in females as in males [55]. "
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