Objective. Volitional modulation of single cortical neurons holds great potential for the implementation of brain–machine interfaces (BMIs) because it can induce a rapid acquisition of arbitrary associations between machines and neural activity. It can also be used as a framework to study the limits of single-neuron control in BMIs. Approach. We tested the control of a one-dimensional actuator in two BMI tasks which differed only in the neural contingency that determined when a reward was dispensed. A thresholded activity task, commonly implemented in single-neuron BMI control, consisted of reaching or exceeding a neuron activity level, while the second task consisted of reaching and maintaining a narrow neuron activity level (i.e. windowed activity task). Main findings. Single neurons in layer V of the motor cortex of rats improved performance during both the thresholded activity and windowed activity BMI tasks. However, correct performance during the windowed activity task was accompanied by activation of neighboring neurons, not in direct control of the BMI. In contrast, only neurons in direct control of the BMI were active at the time of reward during the thresholded activity task. Significance. These results suggest that thresholded activity single-neuron BMI implementations are more appropriate compared to windowed activity BMI tasks to capitalize on the adaptability of cortical circuits to acquire novel arbitrary skills.