Asymmetries in upper limb position sense have been explained in the context of a left limb advantage derived from differences in hemispheric specialization in the processing of kinesthetic information. However, it is not clearly understood how the comparison of perceptual information associated with passive limb displacement and the corresponding matching movement resulting from the execution of a motor command contributes to these differences. In the present study, upper limb position sense was investigated in 12 right-hand-dominant young adults performing wrist position matching tasks which varied in terms of interhemispheric transfer, memory retrieval and whether the reference position was provided by the same or opposite limb. Right and left hand absolute matching errors were similar when the reference and matching positions were produced by the same hand but were 36% greater when matching the reference position with the opposite hand. When examining the constant errors generated from matching movements made with the same hand that provided the reference, the right and left hand matching errors (approximately 3 degrees) were similar. However, when matching with the opposite limb, a large overshoot (P < 0.05) characterized the error when the right hand matched the left hand reference while a large undershoot (P < 0.05) characterized the error when the left hand matched the right hand reference. The overshoot and undershoot were of similar magnitude (approximately 4 degrees). Although asymmetries in the central processing of proprioceptive information such as interhemispheric transfer may exist, the present study suggests that asymmetries in position sense predominantly result from a difference in the "gain of the respective proprioceptive sensory-motor loops". This new hypothesis is strongly supported by a dual-linear model representing the right and left hand sensory-motor systems as well as morphological and physiological data.