Impaired structural connectivity between dorsal attention network and pulvinar mediates the impact of premature birth on adult visual–spatial abilities

Abstract

The dorsal attention network (DAN), including frontal eye fields and posterior parietal cortices, and its link with the posterior thalamus, contribute to visual–spatial abilities. Very premature birth impairs both visual–spatial abilities and cortico‐thalamic structural connectivity. We hypothesized that impaired structural DAN‐pulvinar connectivity mediates the effect of very premature birth on adult visual–spatial abilities. Seventy very premature (median age 26.6 years) and 57 mature born adults (median age 26.6 years) were assessed with cognitive tests and diffusion tensor imaging. Perceptual organization (PO) index of the Wechsler Adult Intelligence Scale‐III was used as a proxy for visual–spatial abilities, and connection probability maps in the thalamus, derived from probabilistic tractography from the DAN, were used as a proxy for DAN‐thalamic connectivity. Premature born adults showed decreases in both PO‐index and connection probability from DAN into the pulvinar, with both changes being positively correlated. Moreover, path analysis revealed that DAN‐pulvinar connectivity mediates the relationship between very premature birth and PO‐index. Results provide evidence for long‐term effects of very premature birth on structural DAN‐pulvinar connectivity, mediating the effect of prematurity on adult visual–spatial impairments. Data suggest DAN‐pulvinar connectivity as a specific target of prognostic and diagnostic procedures for visual–spatial abilities after premature birth.

Involvement of the dorsal and ventral attention networks in visual attention span

“…The current result of more robust activation in ROIs of DAN as compared to that of VAN in VAS-related processing was consistent with the results of previous studies (Lobier et al, 2012(Lobier et al, , 2014. Since the close relationship between top-down (or endogenous) attention and DAN (Berndt et al, 2019;Corbetta & Shulman, 2002), the present finding was generally consistent with the study of Valdois et al (2019), revealing that VAS skills greatly relate to endogenous attention as compared to exogenous attention. The flexible-attention framework proposed by Zhang and Kay (2020) provided a possible explanation for this finding.…”

“…Bottom-up and top-down attentional processes have (partially) separate mechanisms in the neural aspect (Corbetta & Shulman, 2002;Weissman & Prado, 2012). Especially, the top-down attentional control (i.e., endogenous attention) mainly relies on the dorsal attention network (DAN) to orient visuospatial attention and to maintain endogenous signals relating to the current task goals, which are classically implicated with the function in brain regions of bilateral frontal eye fields (FEF) and bilateral posterior parietal cortex (Berndt et al, 2019;Corbetta & Shulman, 2002); meanwhile, dorsolateral prefrontal cortex and portions of dorsal anterior cingulate cortex have also been reported to be recruited in the related control processes (Orr & Weissman, 2009;Weissman & Prado, 2012). In contrast, the stimulus-driven attention (i.e., exogenous attention) remarkably activates the ventral attention network (VAN) to reorient the visuospatial attention, which mainly evokes brain activities in inferior frontal gyrus (IFG), temporoparietal junctions (TPJs), especially in the right hemisphere (Corbetta & Shulman, 2002).…”

Within amygdala: Basolateral parts are selectively impaired in premature-born adults

“…cortico-thalamic structural connectivity, and subcortical grey matter structures, e.g. multi-nuclei structures such as thalamus and neuromodulatory nuclei such as basal cholinergic forebrain, with most of these structural changes being linked with adverse neurodevelopmental outcomes ( Ball et al, 2013 , Berndt et al, 2019 , Eikenes et al, 2011 , Grothe et al, 2017 , Hedderich et al, 2019 , Hedderich et al, 2020a , Hedderich et al, 2020b , Menegaux et al, 2020 , Menegaux et al, 2021 , Meng et al, 2016 , Northam et al, 2011 , Nosarti et al, 2002 , Nosarti et al, 2008 , Pascoe et al, 2019 , Rimol et al, 2019 , Schmitz‐Koep et al, 2020 , Skranes et al, 2007 , Skranes et al, 2013 ). One subcortical grey matter structure of particular interest is the amygdala, which is thought to mediate the brain’s stress response to environmental stressors in the context of premature birth ( Chau et al, 2019 , Scheinost et al, 2016 , Schmitz-Koep et al, 2021 ).…”

Decreased amygdala volume in adults after premature birth

“…For example, very premature-born adults, i.e. born very preterm (VP) before 32 weeks of GA and/or with very low birth weight (VLBW) below 1500 g, have on average more than 10 points lower full-scale IQ scores compared to full-term (FT) controls, which is mediated by aberrant development of distinct brain structures or processes such as cortical folding, white matter integrity and subcortical grey matter volume [5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23] . Causes of aberrant brain development are inflammatory, hypoxic-ischemic and/or stress-related events, which not only affect vulnerable developmental processes, for example pre-oligodendrocyte or subplate neuron (SPN) development at microscopic level [24][25][26] , but also lead to altered macroscopic brain development such as cortical gyri development or white matter integrity 7,8,10,12,15,18,27,28 .…”