Quantifying motor and cortical responses to perturbations during seated locomotor tasks such as recumbent stepping and cycling will expand and improve the understanding of locomotor adaptation processes beyond just perturbed gait. Using a perturbed recumbent stepping protocol, we hypothesized motor errors and anterior cingulate activity would decrease with time, and perturbation timing would influence electrocortical elicitation. Young adults (n = 17) completed four 10-minute arms and legs stepping tasks, with perturbations applied at every left or right leg extension-onset or mid-extension. A random no-perturbation "catch" stride occurred in every five perturbed strides. We instructed subjects to follow a pacing cue and to step smoothly, and we quantified temporal and spatial motor errors. We used high-density electroencephalography to estimate sources of electrocortical fluctuations shared among >70% of subjects. Temporal and spatial errors did not decrease from early to late for either perturbed or catch strides. Interestingly, spatial errors post-perturbation did not return to pre-perturbation levels, suggesting use-dependent learning occurred. Theta (3-8 Hz) synchronization in the anterior cingulate cortex and left and right supplementary motor areas (SMA) emerged near the perturbation event, and extension-onset perturbations elicited greater theta-band power than mid-extension perturbations. Even though motor errors did not adapt, anterior cingulate theta synchronization decreased from early to late perturbed strides, but only during the right-side tasks. Additionally, SMA mainly demonstrated specialized, not contralateral, lateralization. Overall, seated locomotor perturbations produced differential theta-band responses in the anterior cingulate and SMAs, suggesting that tuning perturbation parameters, e.g., timing, can potentially modify electrocortical responses.