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Brain Wiring and Supragranular-Enriched Genes Linked to Protracted Human Frontal Cortex Development.

ABSTRACT: The human frontal cortex is unusually large compared with many other species. The expansion of the human frontal cortex is accompanied by both connectivity and transcriptional changes. Yet, the developmental origins generating variation in frontal cortex circuitry across species remain unresolved. Nineteen genes that encode filaments, synapse, and voltage-gated channels are especially enriched in the supragranular layers of the human cerebral cortex, which suggests enhanced corticocortical projections emerging from layer III. We identify species differences in connections with the use of diffusion MR tractography as well as gene expression in adulthood and in development to identify developmental mechanisms generating variation in frontal cortical circuitry. We demonstrate that increased expression of supragranular-enriched genes in frontal cortex layer III is concomitant with an expansion in corticocortical pathways projecting within the frontal cortex in humans relative to mice. We also demonstrate that the growth of the frontal cortex white matter and transcriptional profiles of supragranular-enriched genes are protracted in humans relative to mice. The expansion of projections emerging from the human frontal cortex arises by extending frontal cortical circuitry development. Integrating gene expression with neuroimaging level phenotypes is an effective strategy to assess deviations in developmental programs leading to species differences in connections.

SUBMITTER: Hendy JP

PROVIDER: S-EPMC7673480 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Environmental enrichment (EE) is widely used in the life sciences to study effects of environment on the brain. In pigs, despite lack of EE being a key welfare issue there is little understanding of brain effects of EE in pigs. This project aimed to study the effects of exposure to an EE arena on piglet behaviours and on brain gene expression levels with a focus on IGF-1 and related genes. Eight litters of large white×landrace×Hampshire piglets were farrowed and raised in a free farrowing system (PigSAFE). At 42days of age, 6pigletsperlitter were given access to an enriched arena with plentiful peat, straw and space, (in groups of 4 made up of stable pairs) for 15min per day on 5 consecutive days to allow them to habituate to the apparatus. Piglet behaviours were recorded in the arena for 15min periods on 3 consecutive days. On the final day only one pair of test piglets per litter was given access to the arena. Brain tissue was collected within 45min of the test from piglets exposed to the arena on the day and their non-exposed littermate controls. RNA was extracted from the frontal cortex and QRT-PCR for selected genes run on a Stratgene MX3005P. In both the home pen and the EE arena litters spent the largest proportion of time engaging in foraging behaviour which was significantly increased in the enriched arena (t7=5.35, df=6, p=0.001). There were decreases in non-running play (t7=4.82, p=0.002) and inactivity (t7=4.6, p=0.002) in the arena. A significant fold change increase (FC=1.07, t=4.42, p=0.002) was observed in IGF-1 gene expression in the frontal cortex of piglets exposed to the enriched arena compared to those not exposed on the day of culling. No change in expression was observed in CSF1, the IGF-1 receptor gene nor in any of the binding proteins tested (IGFBP1-6). There was a weak tendency for increased expression of the neurotrophic factor BDNF1 (fold change: 1.03; t7=1.54, p=0.1). We believe this work is the first to explore effects of EE on pig brain physiology and development, and also points to a potential role for IGF-1 in brain effects of EE.

Dataset Information

Brain Wiring and Supragranular-Enriched Genes Linked to Protracted Human Frontal Cortex Development.

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