Altered cortical gyrification in adults who were born very preterm and its associations with cognition and mental health

Abstract

Background The last trimester of pregnancy is a critical period for the establishment of cortical gyrification and altered folding patterns have been reported following very preterm birth (< 33 weeks of gestation) in childhood and adolescence. However, research is scant on the persistence of such alterations in adulthood and their associations with cognitive and psychiatric outcomes.Methods We studied 79 very-preterm adults and 81 age-matched full-term controls. T1-weighted images were used to measure local gyrification index (LGI), indicating the degree of folding across multiple vertices of the reconstructed cortical surface. Group and group-sex LGI differences were assessed using per-vertex adjustment for cortical thickness and overall intracranial volume. Withingroup correlations were also computed between LGI and functional outcomes, including general intelligence (IQ) and psychopathology.Results Very preterm adults had significantly reduced LGI in extensive cortical regions encompassing the frontal, anterior temporal and occipito-parietal lobes. Alterations in lateral frontotemporal-parietal and medial occipito-parietal regions were present in both males and females, although males reported more extensive alterations. In both very preterm adults and controls, higherLGI was associated with higher IQ and lower psychopathology scores, with the spatial distribution of these associations substantially differing between the two groups.Conclusions Very preterm adults' brains are characterized by significant and widespread local hypogyria and these abnormalities might be implicated in cognitive and psychiatric outcomes.Gyrification reflects an early developmental process and provides a fingerprint for very preterm birth.

Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia

“…Our results converge with previous research demonstrating differences in local folding patterns in cingulate and temporal regions 9 , 10 , 37 , 52 and empirically integrates these spatially localized differences in support of hypotheses of aberrant fronto-temporal and salience network connectivity underpinning the experience of hallucinations in schizophrenia 15 – 17 , 53 . We advance prior research on sulcal asymmetries in the general population and in developmental and psychiatric disorders 21 , 25 – 28 , 30 , 36 , showing a reduction of the typical leftward PCS asymmetry in schizophrenia patients with hallucinations, due to a shorter left hemisphere PCS, compared to patients without hallucinations and to healthy controls. The rightward STS asymmetry was also lower, with a significantly diminished mean depth of the right STS in H+ patients compared to HCs.…”

“…We hypothesize that auditory hallucinations in schizophrenia patients, and the accompanying patterns of brain function, result from alterations to the maturational trajectories in temporal and cingulate regions, and thus their structural covariance. Mechanistic predictions follow, including the role of genes involved in driving the maturational trajectories of cortical patterning 64 and the impact of events that disrupt fetal neurodevelopment 20 , 21 , 62 , 63 . Longitudinal studies following prenatal cohorts until adult life will be required to establish such predictions.…”

“…Mounting evidence suggests that structural covariance networks reflect developmental coordination between brain regions, such that areas with highly correlated anatomical properties, like gyrification, result from similarities in their maturational trajectories 18 , 19 . Although the cellular mechanisms that underlie patterns of cortical covariance remain poorly understood, neurodevelopmental events that influence structural covariance networks significantly affect postnatal outcomes and higher cognitions in adult life 20 , 21 . Structural covariance networks have previously predicted transition to psychosis among individuals at high clinical risk 22 , have demonstrated reduced salience and fronto-parietal control networks in schizophrenia patients compared to healthy controls 23 , and have been shown to have a positive association between frontal–temporal grey matter and auditory hallucination severity in schizophrenia 24 .…”

Temporally and sex‐specific effects of maternal perinatal stress on offspring cortical gyrification and mood in young adulthood

“…Altered LGI has been reported in children (Kesler et al, 2006; Zhang et al, 2015), adolescents (Ganella et al, 2015) as well as adults (Papini et al, 2020) who were born very preterm and the functional consequences of altered LGI has been demonstrated by Papini et al (2020) who reported association between higher LGI and higher IQ and lower psychopathology scores in both very preterm and control adults. LGI is also altered in psychiatric disorders with a prominent neurodevelopmental component.…”

Deviant cortical sulcation related to schizophrenia and cognitive deficits in the second trimester

“…Preterm birth, known to be linked to aberrant in utero cortical development, is associated with defects in cortical folding that appear to persist in adult life [ 4 ]. Aberrant cortical folding in adults related to preterm birth relates to negative cognitive and mental health outcomes [ 4 ].…”