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Early social adversity (ESA) is associated with an increased risk for psychopathology and behavioural problems, but the neurodevelopmental and cognitive pathways underlying this across development remain unclear. One mechanism through which this may occur is via poor development of executive processes. In particular, poor executive function is hypothesized to underlie many negative consequences of early social deprivation, where socio-cognitive stimulation and learning opportunities with a sensitive caregiver are limited or absent (Wade et al., 2022). Accordingly, we adopted a rhesus macaque model of early social deprivation to: i) investigate ESA-effects on executive function longitudinally across adolescence, a time where much development of executive function takes place and risk for psychopathology and antisocial behaviour increases, into adulthood; and ii) identify how the development of specific neural circuits may underlie these relationships. To achieve this, we assessed executive function in two groups of rhesus macaque monkeys differing in exposure to early psychosocial deprivation; one mother-reared (non-ESA-exposed) and one peer-reared (ESA-exposed; i.e. apart from their mothers and other adults from birth) (Shannon et al., 1998); at two time-points corresponding to adolescence (3.5 years) and early adulthood (5 years). We used a version of the ‘A-not-B’ paradigm often used with human infants (Holmboe et al., 2018), with animals completing the task in a section of their home enclosure. At the same time-points we also collected anatomical (T1 and T2) and diffusion MRI. Results revealed that the peer-reared group performed significantly worse on the A not B task at both time-points, with the fitting of a computational model of decision making to the choices of each subject also yielding novel insights into the functional decomposition of group-level executive function differences underlying the performance effect. More specifically, the fitted model parameters showed that while both working memory and response inhibition may be negatively impacted by early social deprivation, the trajectory of development for these two components of executive function differ after exposure to early adversity. In terms of structural brain connectivity, interesting differences between the rearing groups were revealed in terms of white matter integrity in brain networks related to executive function (e.g. the superior longitudinal fasciculus). These differences predicted performance on the A not B task and fitted parameters from the computational model. These findings suggest that early social deprivation specifically has long-term negative effects on executive function via structural changes in the brain, which likely plays a crucial role in the mental health and social difficulties often seen in the context early adversity.
Alice Massera, Institut des Sciences Cognitives - Marc Jeannerod, CNRS/ Université Claude Bernard - Lyon 1
Presenting Author
James Bonaiuto, Institut des Sciences Cognitives-Marc Jeannerod, CNRS
Hind Errame
Mathilda Froesel
Maëva Gacoin
Marine Gautier-Martins
Sara Costa
Suliann Ben Hamed
Bassem Hiba
Holly Rayson, Institut des Sciences Cognitives Marc Jeannerod, CNRS
Pier Ferrari, Institut des Sciences Cognitives-Marc Jeannerod, CNRS