Organisms’ behaviors and perceptions are shaped by the manner in which the brain processes incoming sensory information. Different sensory streams of the brain manage and process disparate types of inputs from sensory receptors in order to transform sensory information into decision and action. To adequately achieve this goal, neurons in many areas simultaneously encode multiple features of the outside world. Jointly encoding various features can, however, lead to ambiguity in the decoding process: single-trial fluctuations in the spike rate of a neuron can represent a change in any or all of the encoded stimulus features. To explore the benefits and impacts of joint coding, we probed the macaque visuomotor pathway. In the first study, we used information theoretic methods to quantify the benefit of joint coding of direction and speed in single neurons in extrastriate area MT, in small simulated populations, and in smooth pursuit eye movements. We found that there is a consistent benefit to encoding multiple stimulus features jointly rather than separately, which we call stimulus synergy. Additionally, we determined that the scale of stimulus synergy can be altered by the tuning bandwidth and the number of stimulus features encoded. The observation of stimulus synergy in pursuit eye movements implies that the MT population is being read out jointly, as a motion vector. In the second study, we further investigated the interaction of direction and speed in pursuit eye movements. We found that single-trial direction and speed errors are correlated, bolstering our claim that fluctuations in the MT population response are jointly decoded to generate direction and speed estimates. Finally, we confirm using simulated MT responses that such correlations can only occur when decoding motion estimates from MT as a motion vector, not as direction and speed separately.