The chronic level of neuromuscular activity, that is, activation and loading, strongly influences the morphological, metabolic, phenotypic, and physiological properties of skeletal muscles. The effects on the innervating motoneurons, however, are less established. We determined and compared the effects of 30 days of decreased activity (induced by a complete mid-thoracic spinal cord transection, ST) or near inactivity (induced by spinal cord isolation, SI) on the soma size and succinate dehydrogenase (SDH) activity of motoneurons innervating a predominantly slow ankle extensor (soleus) and a predominantly fast ankle flexor (tibialis anterior) muscle of adult rats. Soleus and tibialis anterior motoneuron pools were labeled retrogradely using nuclear yellow. The alpha- and gamma-motoneurons were classified based on soma size. Mean number of labeled motoneurons, and mean soma size and SDH activity for both alpha- and gamma-motoneurons were similar in control, ST, and SI rats. Compared to previous reports showing significant decreases in muscle fiber size and adaptations toward a "faster" metabolic profile following ST and SI, the results indicate that, unlike the muscles they innervate, the motoneurons are relatively unresponsive to chronic reductions in neuromuscular activity. The implication of these results is that mean size and SDH activity are independent of the number of action potentials generated by both alpha- and gamma-motoneurons and that even the absence of afferent input to the spinal cord has no influence on size and oxidative metabolic potential of the motoneuron soma.