Task errors are used to learn and refine motor skills. We investigated how task assistance influences learned neural representations using Brain-Computer Interfaces (BCIs), which map neural activity into movement via a decoder. We analyzed motor cortex activity as monkeys practiced BCI with a decoder that adapted to improve or maintain performance over days. Over time, task-relevant information became concentrated in fewer neurons, unlike with fixed decoders. At the population level, task information also became largely confined to a few neural modes that accounted for an unexpectedly small fraction of the population variance. A neural network model suggests the adaptive decoders directly contribute to forming these more compact neural representations. Our findings show that assistive decoders manipulate error information used for long-term learning computations like credit assignment, which informs our understanding of motor learning and has implications for designing real-world BCIs.