Save your friend, strike your enemy! How sex and handedness influence EEG signatures of cooperative and competitive behaviour

Some evolutionary theories explain population-level right vs left motor asymmetries in accordance with the achievement of equilibrium in social cooperation and competition. In humans, an Evolutionarily Stable Strategy (ESS) suggests that left/right-handers would be more efficient in competitive/cooperative behaviours, respectively, with stronger asymmetry expected in males. To test one facet of the ESS, we recorded electroencephalography (EEG) prior (rest-EEG) and during a Go/NoGo task in which 24 left- and 24 right-handed participants (half females) press a key (Go condition) to either “save a friend” (cooperation) or “hit an enemy” (competition). This ‘rapid decision’ paradigm assess neural and behavioral dynamics of action initiation and inhibition in a socially valenced context. Accuracy was higher in males than females, and response times were faster in the enemy than friend condition. Rest-EEG showed higher beta relative power at both frontal and parietal sites for females compared to males, but only in left-handers. The expected frontal alpha asymmetry was not found. Frontal N2 latency confirmed faster peaks for Go vs. NoGo trials in left/right-handed females in the enemy/friend condition, respectively, in accordance with the ESS. In males, a faster frontal N2 was recorded for Go compared to NoGo trials in the enemy condition in both left- and right-handers; moreover, the P3 at frontal and parietal sites revealed interactions among handedness, condition and hemisphere, showing that the left/right hemispheres of males seem to be more attuned to cooperative/competitive stimuli, respectively. Results are discussed in the view of evolutionary theories on population-level lateralization and approach/avoidance hemispheric specialization.