Background Parasternal intercostal is an obligatory inspiratory muscle working in coordination with the diaphragm, apparently sharing a common pathway of neural response. This similarity has attracted clinical interest, promoting parasternal as a non-invasive alternative to the diaphragm, to monitor central neural respiratory output. However, this role may be confounded by the distinct and different functions of costal and crural diaphragm. Given the anatomic location, parasternal activation may significantly impact chest wall via both mechanical shortening or as a "fixator" for the chest wall. Either mechanical function of parasternal may also impact differential function of costal and crural. Objectives During eupnea and hypercapnia, 1) compare the intensity of neural activation of parasternal, with costal and crural diaphragm; 2)examine parasternal recruitment and changes in mechanical action during progressive hypercapnia, including muscle baseline length and shortening. Methods In 30 spontaneously breathing canines, awake without confounding anesthetic, we measured directly both electrical activity of parasternal, costal, and crural diaphragm, and corresponding mechanical shortening of parasternal, during eupnea and hypercapnia. Results During eupnea and hypercapnia, parasternal and costal diaphragm share a similar intensity of neural activation, while both differ significantly from crural diaphragm activity. The shortening of parasternal increases significantly with hypercapnia, without change in baseline end-expiratory length. Conclusion Parasternal shares an equivalent intensity of neural activation with costal, but not crural, diaphragm. Parasternal maintains and increases its active inspiratory shortening during augmented ventilation, despite high levels of diaphragm recruitment. Throughout hypercapnic ventilation, parasternal contributes mechanically - it is not relegated to chest wall fixation.