Neonatal surgical injury alters social behaviour and cortical network responses to adult incision

Abstract

Early-life painful events can influence brain development and behaviour later in life, yet the neural mechanisms underlying these long-term effects remain poorly understood. In particular, exposure to pain or tissue injury during early postnatal life has been associated with altered sensory processing, emotional regulation and behavioural responses later in life. Here we investigated whether early-life surgical pain alters adult behavioural and cortical network responses to injury. Using a rat model of neonatal hindpaw incision followed by repeat adult surgical incision, we combined behavioural analysis with continuous electrophysiological recordings from the medial prefrontal cortex (mPFC) and primary somatosensory cortex (S1) in freely moving animals. Early-life incision did not produce an overt alteration in adult social behaviour under baseline conditions. However, following adult injury, rats with prior neonatal incision showed altered social behavioural responses compared with animals receiving an incision only in adulthood. At the network level, adult incision increased beta-gamma phase-amplitude coupling within the mPFC and S1-mPFC theta coherence in animals experiencing their first injury, but not in those incised neonatally. Our evidence indicates that the relationship between mPFC coupling and social interaction differed according to neonatal injury history, revealing a lasting reorganisation of cortical network recruitment and brain-behaviour coupling after repeat injury.